MUC1 in human and murine mammary carcinoma cells decreases the expression of core 2 β1,6-N-acetylglucosaminyltransferase and β-galactoside α2,3-sialyltransferase

Glycobiology

Volumn 22, Issue 8, 2012, Pages 1042-1054

  Solatycka, Alicja ^a   Owczarek, Tomasz ^a,b   Piller, Friedrich ^c   Piller, Véronique ^c   Pula, Bartosz ^d   Wojciech, Lukasz ^b   Podhorska Okolow, Marzena ^d   Dziegiel, Piotr ^d,e,f   Ugorski, Maciej ^a,b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b WROCLAW UNIVERSITY OF ENVIRONMENTAL AND LIFE SCIENCES   (Poland)

^c UNIVERSITÉ D'ORLÉANS   (France)

^d WROCLAW MEDICAL UNIVERSITY   (Poland)

^e POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

^f UNIVERSITY OF WROC AW   (Poland)

Author keywords

Adhesion; Breast cancer; C2GnT1; MUC1; ST3Gal I

Indexed keywords

BETA GALACTOSIDE ALPHA2,3 SIALYLTRANSFERASE; CORE 1 BETA 1,3 GALACTOSYLTRANSFERASE; CORE 2 BETA 1,6 N ACETYLGLUCOSAMINYLTRANSFERASE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GALACTOSYLTRANSFERASE; GLYCAN; MESSENGER RNA; MUCIN 1; N ACETYLGLUCOSAMINYLTRANSFERASE; OLIGOSACCHARIDE; SHORT HAIRPIN RNA; SIALYL LEWIS X ANTIGEN; SIALYLTRANSFERASE; T LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CARCINOMA CELL; CELL ADHESION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; GENE VECTOR; GENETIC ASSOCIATION; GENETIC TRANSFECTION; GROWTH INHIBITION; HUMAN; HUMAN CELL; MEDIATOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RECEPTOR DOWN REGULATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; BLOTTING, WESTERN; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL ADHESION; E-SELECTIN; FEMALE; FLOW CYTOMETRY; GALACTOSYLTRANSFERASES; GALECTIN 3; GLYCOSYLATION; HUMANS; IMMUNOENZYME TECHNIQUES; MICE; MUCIN-1; N-ACETYLGLUCOSAMINYLTRANSFERASES; N-ACETYLNEURAMINIC ACID; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIALYLTRANSFERASES; TUMOR CELLS, CULTURED;

MURINAE;

EID: 84863195565     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cws075     Document Type: Article

References (59)

1. Amano J, Straehl P, Berger EG, Kochibe N, Kobata A. 1991. Structures of mucin-type sugar chains of the galactosyltransferase purified from human milk. Occurrence of the ABO and Lewis blood group determinants. J Biol Chem. 266:11461-11477. (Pubitemid 21906973)
2. Baldus SE, Hanisch FG, Kotlarek GM, Zirbes TK, Thiele J, Isenberg J, Karsten UR, Devine PL, Dienes HP. 1998. Coexpression of MUC1 mucin peptide core and the Thomsen-Friedenreich antigen in colorectal neoplasms. Cancer. 82:1019-1027. (Pubitemid 28136513)
3. Baldus SE, Hanisch FG, Monaca E, Karsten UR, Zirbes TK, Thiele J, Dienes HP. 1999. Immunoreactivity of Thomsen-Friedenreich (TF) antigen in human neoplasms: The importance of carrier-specific glycotope expression on MUC1. Histol Histopathol. 14:1153-1158. (Pubitemid 29447456)
4. Bevilacqua MP, Nelson RM, Mannori G, Cecconi O. 1994. Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med. 45:361-378. (Pubitemid 24158168)
5. Bierhuizen MFA, Fukuda M. 1992. Expression cloning of a cDNA encoding UDP-GlcNAc:Galbeta1-3GalNAc-R(GlcNAc-to-GalNAc)beta1-6GlcNac transferase by gene transfer into CHO cells expressing polyoma large tumor antigen. Proc Natl Acad Sci USA. 89:9326-9330.
6. Brockhausen I. 1999. Pathways of O-glycan biosynthesis in cancer cells. Biochim Biophys Acta. 1473:67-95.
7. Brockhausen I. 2006. Mucin-type O-glycans in human colon and breast cancer: Glycodynamics and functions. EMBO Rep. 7:599-604. (Pubitemid 43827326)
8. Brockhausen I, Yang J, Burchell J, Whitehouse C, Taylor-Papadimitriou J. 1995. Mechanism underlying aberrant glycosylation of the MUC1 mucin in breast cancer cells. Eur J Biochem. 233:607-617.
9. Burchell JM, Mungul A, Taylor-Papadimitriou J. 2001. O-linked glycosylation in the mammary gland: Changes that occur during malignancy. J Mammary Gland Biol Neoplasia. 6:355-364.
10. Burchell J, Poulsom R, Hanby A, Whitehouse C, Cooper L, Clausen H, Miles D, Taylor-Papadimitriou J, 1999. An α2,3 sialyltransferase (ST3Gal I) is elevated in primary breast carcinomas. Glycobiology. 9:1307-1311. (Pubitemid 30011510)
11. Croce MV, Isla-Larrain MT, Demichelis SO, Gori JR, Price MR, Segal-Eiras A. 2003. Tissue and serum MUC1 mucin detection in breast cancer patients. Breast Cancer Res Treat. 81:195-207. (Pubitemid 37352457)
12. Dahiya R, Itzkowitz SH, Byrd JC, Kim YS. 1992. Mucin oligosaccharide biosynthesis in human colonic cancerous tissues and cell lines. Cancer. 70:1467-1476.
13. Dalziel M, Whitehouse C, McFarlane I, Brockhausen, Gschmeissner S, Schwientek T, Clausen H, Burchell J, Taylor-Papadimitriou J. 2001. The relative activities of the C2GnT1 and ST3Gal I glycosyltransferases determine O-glycan structure and expression of a tumor-associated epitope on MUC1. J Biol Chem. 276:11007-11015. (Pubitemid 38089281)
14. Duk M, Steuden I, Duś D, Radzikowski C, Lisowska E. 1992. Application of chemically desialylated and degalactosylated human glycophorin for induction and characterization of anti-Tn monoclonal antibodies. Glycoconjugate J. 9:148-153.
15. Elston CW, Ellis IO. 1991. Pathological prognostic factors in breast cancer: Experience from a large study with long-term follow-up. Histopathology. 19:403-410.
16. Fukuda M. 1996. Possible roles of tumor-associated carbohydrate antigens. Cancer Res. 56:2237-2244. (Pubitemid 26154066)
17. Gendler SJ. 2001. MUC1, the renaissance molecule. J Mammary Gland Biol Neoplasia. 6:339-353.
18. Hanisch FG, Baldus SE. 1997. The Thomsen-Friedenreich antigen: A critical review on the structural, biosynthetic and histochemical aspects of a pancarcinoma-associated antigen. Histol Histopathol. 12:263-281.
19. Hanisch FG, Stadie TR, Deutzmann F, Peter-Katalinic J. 1996. MUC1 glycoforms in breast cancer-cell line T47D as a model for carcinoma-associated alterations of O-glycosylation. Eur J Biochem. 236:318-327. (Pubitemid 26074885)
20. Hanisch FG, Uhlenbruck G, Peter-Katalinic J, Egge H, Dabrowski J, Dabrowski U. 1989. Structures of neutral O-linked polylactosaminoglycans on human skim milk mucins. A novel type of linearly extended poly-N- acetyllactosamine backbones with Galß(1-6) repeating units. J Biol Chem. 264:872-883.
21. Hollingsworth MA, Swanson BJ. 2004. Mucins in cancer: Protection and control of the cell surface. Nature Rev Cancer. 4:45-60. (Pubitemid 38082153)
22. Huang L, Chen D, Liu D, Yin L, Kharbanda S, Kufe D. 2005. MUC1 oncoprotein blocks glycogen synthase kinase 3β-mediated phosphorylation and degradation of β-catenin. Cancer Res. 65:10413-10422. (Pubitemid 41743735)
23. Huang MC, Chen HY, Huang HC, Huang J, Liang JT, Shen TL, Lin NY, Ho CC, Cho IM, Hsu SM. 2006. C2GnT-M is downregulated in colorectal cancer and its re-expression causes growth inhibition of colon cancer cells. Oncogene. 25:3267-3276. (Pubitemid 43846311)
24. Hull SR, Bright A, Carraway KL, Abe M, Hayes DF, Kufe DW. 1989. Oligosaccharide differences in the DF3 sialomucin antigen from normal human milk and the BT-20 human breast carcinoma cell line. Cancer Commun. 1:261-267.
25. Ju T, Brewer K, D'Souza A, Cummings RD, Canflield WM. 2002. Cloning and expression of human core 1 β1,3-galactosyltransferase. J Biol Chem. 277:178-186. (Pubitemid 34952043)
26. Kawano T, Ahmad R, Nogi H, Agata N, Anderson K, Kufe D. 2008. MUC1 oncoprotein promotes growth and survival of human myeloma cells. Int J Oncol. 33:153-159.
27. Khodarev NN, Pitroda SP, Beckett MA, MacDermed DM, Huang L, Kufe DW, Weichselbaum RR. 2009. MUC1-induced transcriptional programs associated withtumorigenesis predict outcome in breast and lung cancer. Cancer Res. 69:2833-2837.
28. Kłopocki AG, Laskowska A, Antoniewicz-Papis J, Duk M, Lisowska E, Ugorski M. 1998. Role of sialosyl Lewisa in adhesion of colon cancer cells-the antisense RNA approach. Eur J Biochem. 253:309-318. (Pubitemid 28182334)
29. Kumamoto K, Goto Y, Sekikawa K, Takenoshita S, Ishida N, Kawakita M, Kannagi R. 2001. Increased expression of UDP-galactose transporter messenger RNA In human colon cancer tissues and its implication in synthesis of Thomsen-Friedenreich antigen and sialyl Lewis A/X determinants. Cancer Res. 61:4620-4627. (Pubitemid 32685798)
30. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
31. Lawrence MB, McIntire LV, Eskin SG. 1987. Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood. 70:1284-1290. (Pubitemid 18026127)
32. Li Y, Bharti A, Chen D, Gong J, Kufe D. 1998. Interaction of glycogen synthase kinase 3β with the DF3/MUC1 carcinoma-associated antigen and β-catenin. Mol Cell Biol. 18:7216-7224. (Pubitemid 28533041)
33. Li Y, Kuwahara H, Ren J, Wen G, Kufe D. 2001. The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3β and β-catenin. J Biol Chem. 276:6061-6064.
34. Ligtenberg MJ, Buijs F, Vos HL, Hilkens J. 1992. Suppression of cellular aggregation by high levels of episialin. Cancer Res. 52:2318-2324.
35. Lloyd KO, Burchell J, Kudryashow V, Yin BW, Taylor-Papadimitriou J. 1996. Comparison of O-linked carbohydrate chains in MUC-1 mucin from normal breast epithelial cell lines and breast carcinoma cell lines. Demonstration of simpler and fewer glycan chains in tumor cells. J Biol Chem. 271:33325-33334. (Pubitemid 27010142)
36. X structures in O-glycans. J Biol Chem. 267:24379-24386.
37. Mahanta S, Fessler SP, Park J, Bamdad C. 2008. A minimal fragment of MUC1 mediates growth of cancer cells. PLoS One. 3:e2054.
38. Mukhopadhyay P, Chakraborty S, Ponnusamy MP, Lakshmanan I, Jain M, Batra SK. 2011. Mucins in the pathogenesis of breast cancer: Implications in diagnosis, prognosis and therapy. Biochim Biophys Acta. 1815:224-240.
39. Piller F, Piller V, Fox RI, Fukuda M. 1988. Human T-lymphocyte activation is associated with changes in O-glycan biosynthesis. J Biol Chem. 263:15146-15150.
40. Raina D, Ahmad R, Kumar S, Ren J, Yoshida K, Kharbanda S, Kufe D. 2006. MUC1 oncoprotein blocks nuclear targeting of c-Abl in the apoptotic response to DNA damage. EMBO J. 25:3774-3783. (Pubitemid 44300263)
41. Ramasamy S, Duraisamy S, Barbashov S, Kawano T, Kharbanda S, Kufe D. 2007. The MUC1 and galectin-3 oncoproteins function in a micro-RNA-dependent regulatory loop. Mol Cell. 27:992-1004. (Pubitemid 47488189)
42. Regimbald LH, Pilarski LM, Longenecker BM, Reddish MA, Zimmermann G, Hugh JC. 1996. The breast mucin MUC1 as a novel adhesion ligand for endothelial intercellular adhesion molecule 1 in breast cancer. Cancer Res. 56:4244-4249. (Pubitemid 26305023)
43. Remmele W, Stegner HE. 1987. Vorschlag zur einheitlichen Definition eines immunreactivn Score (IRS) fuer den immunohistochemischen Ostrogenrezeptor- Nachweis (ER-ICA) im Mammakarzinomgewebe. Pathologe. 8:138-140.
44. Ren J, Li Y, Kufe D. 2002. Protein kinase Cδ regulates function of the DF3/MUC1 carcinoma antigen in β-catenin signaling. J Biol Chem. 277:17616-17622. (Pubitemid 34967564)
45. Schneider F, Kemmer W, Haensch W, Franke G, Gretschel S, Karsten U, Schlag PM. 2001. Overexpression of sialyltransferase CMP-sialic acid: Galß1,3GalNAc-R α6-sialyltransferase is related to poor patient survival in human colorectal carcinomas. Cancer Res. 61:4605-4611. (Pubitemid 32685796)
46. Schwientek T, Yeh J-C, Levery SB, Keck B, Merkx G, van Kessel AG, Fukuda M, Clausen H. 2000. Control of O-glycan branch formation: Molecular cloning and characterization of a novel thymus-associated core 2 β1,6-N- acetylglucosaminyltransferase. J Biol Chem. 275:11106-11113. (Pubitemid 30212753)
47. Steuden I, Duk M, Czerwiñski M, Radzikowski C, Lisowska E. 1985. The monoclonal antibody, anti-asialoglycophorin from human erythrocytes, specific for β-D-Gal-1-3-α-D-GalNAc-chains (Thompson-Friedenreich receptors). Glycoconjugate J. 2:303-314. (Pubitemid 15235412)
48. Taylor-Papadimitriou J, Burchell J, Miles DW, Dalziel M. 1999. MUC1 and cancer. Biochim Biophys Acta. 1455:301-313. (Pubitemid 29435996)
49. Wei X, Xu H, Kufe D. 2005. Human MUC1 oncoprotein regulates p53-responsive gene transcription in the genotoxic stress response. Cancer cell. 7:167-178. (Pubitemid 40248342)
50. Wei X, Xu H, Kufe D. 2006. MUC1 oncoprotein stabilizes and activates estrogen receptor alpha. Mol Cell. 21:295-305. (Pubitemid 43099944)
51. Wessling J, van der Valk SW, Vos HL, Sonnenberg A, Hikens J, Episialin . 1995. MUC1 overexpression inhibits integrin-mediated cell adhesion to extracellular matrix components. J Cell Biol. 129:255-265.
52. Wolf MF, Ludwig A, Fritz P, Schumacher K. 1988. Increased expression of Thomsen-Friedenreich antigens during tumor progression in breast cancer patients. Tumour Biol. 9:190-194.
53. Yanagihara K, Seki M, Cheng PW. 2001. Lipopolysaccharide Induces Mucus Cell Metaplasia in Mouse Lung. Am J Respir Cell Mol Biol. 24:66-73. (Pubitemid 32097509)
54. Yeh J-C, Ong E, Fukuda M. 1999. Molecular cloning and expression of a novel β1,6-N-acetylglucoaminyltransferase that forms core 2, core 4 and I branches. J Biol Chem. 274:3215-3221. (Pubitemid 29075411)
55. Yu L-G. 2007. The oncofetal Thomsen-Friedenreich carbohydrate antigen in cancer progression. Glycoconj J. 24:411-420. (Pubitemid 47512574)
56. Yu L-G, Andrews N, Zhao Q, McKean D, Williams JF, Connor LJ, Gerasimenko OV, Hilkens J, Hirabayashi J, Kasai K, et al. 2007. Galectin- 3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J Biol Chem. 282:773-781. (Pubitemid 47076627)
57. Zhang K, Baeckstrom D, Brevinge H, Hansson GC. 1996. Secreted MUC1 mucins lacking their cytoplasmic part and carrying sialyl-Lewis a and x epitopes from a tumor cell line and sera of colon carcinoma patients can inhibit HL-60 leukocyte adhesion to E-selectin-expressing endothelial cells. J Cell Biochem. 60:538-549. (Pubitemid 26112066)
58. Zhao Q, Guo X, Nash GB, Stone PC, Hilkens J, Rhodes JM, Yu LG. 2009. Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res. 69:6799-6806.
59. Zotter S, Hageman PC, Lossnitzer A, Mooi WJ, Hilgers J. 1988. Tissue and tumor distribution of human polymorphic epithelial mucin. Cancer Rev. 11/12:55-101. (Pubitemid 19206475)