Aberrantly glycosylated MUC1 is expressed on the surface of breast cancer cells and a target for antibody-dependent cell-mediated cytotoxicity

Glycoconjugate Journal

Volumn 30, Issue 3, 2013, Pages 227-236

  Lavrsen, Kirstine ^a   Madsen, Caroline B ^a   Rasch, Morten G ^b   Woetmann, Anders ^a   Ødum, Niels ^a   Mandel, Ulla ^a   Clausen, Henrik ^a   Pedersen, Anders E ^a   Wandall, Hans H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b FINSEN LABORATORY   (Denmark)

Author keywords

ADCC; Antibodies; Cancer; GalNAc; Glycans; Glycopeptide; Immunotherapy; MUC1

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 5E5; MUCIN 1; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BINDING AFFINITY; BREAST CANCER; CANCER CELL; CELL SURFACE; COMPLEMENT DEPENDENT CYTOTOXICITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION;

ACETYLGALACTOSAMINE; ADENOCARCINOMA; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; BREAST NEOPLASMS; FEMALE; GLYCOSYLATION; HUMANS; MCF-7 CELLS; MUCIN-1;

MUS;

EID: 84876473766     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-012-9437-7     Document Type: Article

References (51)

1. Singh, P.K., Hollingsworth, M.A.: Cell surface-associated mucins in signal transduction. Trends Cell Biol. 16(9), 467-476 (2006)
2. Taylor-Papadimitriou, J., Burchell, J.M., Plunkett, T., Graham, R., Correa, I., Miles, D., Smith, M.: MUC1 and the immunobiology of cancer. J. Mammary Gland Biol. Neoplasia 7(2), 209-221 (2002)
3. Sorensen, A.L., Reis, C.A., Tarp, M.A., Mandel, U., Ramachandran, K., Sankaranarayanan, V., Schwientek, T., Graham, R., Taylor-Papadimitriou, J., Hollingsworth, M.A., et al.: Chemoenzymatically synthesized multimeric Tn/STn MUC1 glycopeptides elicit cancer-specific anti-MUC1 antibody responses and override tolerance. Glycobiology 16(2), 96-107 (2006)
4. Lloyd, K.O., Burchell, J., Kudryashov, V., Yin, B.W., Taylor-Papadimitriou, J.: 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(52), 33325-33334 (1996)
5. Tarp, M.A., Clausen, H.: Mucin-type O-glycosylation and its potential use in drug and vaccine development. Biochim. Biophys. Acta 1780(3), 546-563 (2008)
6. Hakomori, S., Yamamura, S., Handa, A.K.: Signal transduction through glyco(sphingo)lipids. Introduction and recent studies on glyco(sphingo)lipid- enriched microdomains. Ann. N. Y. Acad. Sci. 845, 1-10 (1998)
7. Springer, G.F.: T and Tn, general carcinoma autoantigens. Science 224(4654), 1198-1206 (1984)
8. Maraveyas, A., Snook, D., Hird, V., Kosmas, C., Meares, C.F., Lambert, H.E., Epenetos, A.A.: Pharmacokinetics and toxicity of an yttrium-90-CITC-DTPA- HMFG1 radioimmunoconjugate for intraperitoneal radioimmunotherapy of ovarian cancer. Cancer 73(3 Suppl), 1067-1075 (1994)
9. DeNardo, S.J., Kramer, E.L., O'Donnell, R.T., Richman, C.M., Salako, Q.A., Shen, S., Noz, M., Glenn, S.D., Ceriani, R.L., DeNardo, G.L.: Radioimmunotherapy for breast cancer using indium-111/yttrium-90 BrE-3: results of a phase I clinical trial. J. Nucl. Med. 38(8), 1180-1185 (1997)
10. Snijdewint, F.G., von Mensdorff-Pouilly, S., Karuntu-Wanamarta, A.H., Verstraeten, A.A., Livingston, P.O., Hilgers, J., Kenemans, P.: Antibody-dependent cell-mediated cytotoxicity can be induced by MUC1 peptide vaccination of breast cancer patients. Int. J. Cancer 93(1), 97-106 (2001)
11. Karanikas, V., Hwang, L.A., Pearson, J., Ong, C.S., Apostolopoulos, V., Vaughan, H., Xing, P.X., Jamieson, G., Pietersz, G., Tait, B., et al.: Antibody and T cell responses of patients with adenocarcinoma immunized with mannan-MUC1 fusion protein. J. Clin. Invest. 100(11), 2783-2792 (1997)
12. Apostolopoulos, V., Pietersz, G.A., Tsibanis, A., Tsikkinis, A., Drakaki, H., Loveland, B.E., Piddlesden, S.J., Plebanski, M., Pouniotis, D.S., Alexis, M.N., et al.: Pilot phase III immunotherapy study in early-stage breast cancer patients using oxidized mannan-MUC1 [ISRCTN71711835]. Breast Cancer Res. 8(3), R27 (2006)
13. Loveland, B.E., Zhao, A., White, S., Gan, H., Hamilton, K., Xing, P.X., Pietersz, G.A., Apostolopoulos, V., Vaughan, H., Karanikas, V., et al.: Mannan-MUC1-pulsed dendritic cell immunotherapy: a phase I trial in patients with adenocarcinoma. Clin. Cancer Res. 12(3 Pt 1), 869-877 (2006)
14. Goydos, J.S., Elder, E., Whiteside, T.L., Finn, O.J., Lotze, M.T.: A phase I trial of a synthetic mucin peptide vaccine. Induction of specific immune reactivity in patients with adenocarcinoma. J. Surg. Res. 63(1), 298-304 (1996)
15. Gilewski, T., Adluri, S., Ragupathi, G., Zhang, S., Yao, T.J., Panageas, K., Moynahan, M., Houghton, A., Norton, L., Livingston, P.O.: Vaccination of high-risk breast cancer patients with mucin-1 (MUC1) keyhole limpet hemocyanin conjugate plus QS-21. Clin. Cancer Res. 6(5), 1693-1701 (2000)
16. von Mensdorff-Pouilly, S., Petrakou, E., Kenemans, P., van Uffelen, K., Verstraeten, A.A., Snijdewint, F.G., van Kamp, G.J., Schol, D.J., Reis, C.A., Price, M.R., et al.: Reactivity of natural and induced human antibodies to MUC1 mucin with MUC1 peptides and n-acetylgalactosamine (GalNAc) peptides. Int. J. Cancer 86(5), 702-712 (2000)
17. Finn, O.J., Jerome, K.R., Henderson, R.A., Pecher, G., Domenech, N., Magarian-Blander, J., Barratt-Boyes, S.M.: MUC-1 epithelial tumor mucin-based immunity and cancer vaccines. Immunol. Rev. 145, 61-89 (1995)
18. Wykes, M., MacDonald, K.P., Tran, M., Quin, R.J., Xing, P.X., Gendler, S.J., Hart, D.N., McGuckin, M.A.: MUC1 epithelial mucin (CD227) is expressed by activated dendritic cells. J. Leukoc. Biol. 72(4), 692-701 (2002)
19. Brugger, W., Buhring, H.J., Grunebach, F., Vogel, W., Kaul, S., Muller, R., Brummendorf, T.H., Ziegler, B.L., Rappold, I., Brossart, P., et al.: Expression of MUC-1 epitopes on normal bone marrow: implications for the detection of micrometastatic tumor cells. J. Clin. Oncol. 17(5), 1535-1544 (1999)
20. Fattorossi, A., Battaglia, A., Malinconico, P., Stoler, A., Andreocci, L., Parente, D., Coscarella, A., Maggiano, N., Perillo, A., Pierelli, L., et al.: Constitutive and inducible expression of the epithelial antigen MUC1 (CD227) in human T cells. Exp. Cell Res. 280(1), 107-118 (2002)
21. Moreno, M., Bontkes, H.J., Scheper, R.J., Kenemans, P., Verheijen, R.H., von Mensdorff-Pouilly, S.: High level of MUC1 in serum of ovarian and breast cancer patients inhibits huHMFG-1 dependent cell-mediated cytotoxicity (ADCC). Cancer Lett. 257(1), 47-55 (2007)
22. Sabbatini, P.J., Ragupathi, G., Hood, C., Aghajanian, C.A., Juretzka, M., Iasonos, A., Hensley, M.L., Spassova, M.K., Ouerfelli, O., Spriggs, D.R., et al.: Pilot study of a heptavalent vaccine-keyhole limpet hemocyanin conjugate plus QS21 in patients with epithelial ovarian, fallopian tube, or peritoneal cancer. Clin. Cancer Res. 13(14), 4170-4177 (2007)
23. Wandall, H.H., Blixt, O., Tarp, M.A., Pedersen, J.W., Bennett, E.P., Mandel, U., Ragupathi, G., Livingston, P.O., Hollingsworth, M.A., Taylor-Papadimitriou, J., et al.: Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer Res. 70(4), 1306-1313 (2010)
24. Pedersen, J.W., Blixt, O., Bennett, E.P., Tarp, M.A., Dar, I., Mandel, U., Poulsen, S.S., Pedersen, A.E., Rasmussen, S., Jess, P., et al.: Seromic profiling of colorectal cancer patients with novel glycopeptide microarray. Int. J. Cancer 128(8), 1860-1871 (2011)
25. Tarp, M.A., Sorensen, A.L., Mandel, U., Paulsen, H., Burchell, J., Taylor-Papadimitriou, J., Clausen, H.: Identification of a novel cancer-specific immunodominant glycopeptide epitope in the MUC1 tandem repeat. Glycobiology 17(2), 197-209 (2007)
26. Kracun, S.K., Clo, E., Clausen, H., Levery, S.B., Jensen, K.J., Blixt, O.: Random glycopeptide bead libraries for seromic biomarker discovery. J. Proteome Res. 9(12), 6705-6714 (2010)
27. Wandall, H.H., Hassan, H., Mirgorodskaya, E., Kristensen, A.K., Roepstorff, P., Bennett, E.P., Nielsen, P.A., Hollingsworth, M.A., Burchell, J., Taylor-Papadimitriou, J., et al.: Substrate specificities of three members of the human UDP-N-acetyl-alpha-D-galactosamine:Polypeptide N- acetylgalactosaminyltransferase family, GalNAc-T1, -T2, and -T3. J. Biol. Chem. 272(38), 23503-23514 (1997)
28. Bennett, E.P., Hassan, H., Clausen, H.: cDNA cloning and expression of a novel human UDP-N-acetyl-alpha-D-galactosamine. Polypeptide N- acetylgalactosaminyltransferase, GalNAc-t3. J. Biol. Chem. 271(29), 17006-17012 (1996)
29. White, T., Bennett, E.P., Takio, K., Sorensen, T., Bonding, N., Clausen, H.: Purification and cDNA cloning of a human UDP-N-acetyl-alpha-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase. J. Biol. Chem. 270(41), 24156-24165 (1995)
30. Ikehara, Y., Kojima, N., Kurosawa, N., Kudo, T., Kono, M., Nishihara, S., Issiki, S., Morozumi, K., Itzkowitz, S., Tsuda, T., et al.: Cloning and expression of a human gene encoding an N-acetylgalactosamine-alpha2,6- sialyltransferase (ST6GalNAc I): a candidate for synthesis of cancer-associated sialyl-Tn antigens. Glycobiology 9(11), 1213-1224 (1999)
31. Kurosawa, N., Takashima, S., Kono, M., Ikehara, Y., Inoue, M., Tachida, Y., Narimatsu, H., Tsuji, S.: Molecular cloning and genomic analysis of mouse GalNAc alpha2, 6-sialyltransferase (ST6GalNAc I). J. Biochem. 127(5), 845-854 (2000)
32. Burchell, J., Gendler, S., Taylor-Papadimitriou, J., Girling, A., Lewis, A., Millis, R., Lamport, D.: Development and characterization of breast cancer reactive monoclonal antibodies directed to the core protein of the human milk mucin. Cancer Res. 47(20), 5476-5482 (1987)
33. Beatson, R.E., Taylor-Papadimitriou, J., Burchell, J.M.: MUC1 immunotherapy. Immunotherapy 2(3), 305-327 (2010)
34. Burchell, J.M., Mungul, A., Taylor-Papadimitriou, J.: O-linked glycosylation in the mammary gland: changes that occur during malignancy. J. Mammary Gland Biol. Neoplasia 6(3), 355-364 (2001)
35. Wang, B.L., Springer, G.F., Carlstedt, S.C.: Quantitative computerized image analysis of Tn and T (Thomsen-Friedenreich) epitopes in prognostication of human breast carcinoma. J. Histochem. Cytochem. 45(10), 1393-1400 (1997)
36. Van Elssen, C.H., Frings, P.W., Bot, F.J., Van de Vijver, K.K., Huls, M.B., Meek, B., Hupperets, P., Germeraad, W.T., Bos, G.M.: Expression of aberrantly glycosylated Mucin-1 in ovarian cancer. Histopathology 57(4), 597-606 (2010)
37. Roda, J.M., Joshi, T., Butchar, J.P., McAlees, J.W., Lehman, A., Tridandapani, S., Carson 3rd, W.E.: The activation of natural killer cell effector functions by cetuximab-coated, epidermal growth factor receptor positive tumor cells is enhanced by cytokines. Clin. Cancer Res. 13(21), 6419-6428 (2007)
38. Dunne, J., Lynch, S., O'Farrelly, C., Todryk, S., Hegarty, J.E., Feighery, C., Doherty, D.G.: Selective expansion and partial activation of human NK cells and NK receptor-positive T cells by IL-2 and IL-15. J. Immunol. 167(6), 3129-3138 (2001)
39. Herberman, R.B., Ortaldo, J.R., Mantovani, A., Hobbs, D.S., Kung, H.F., Pestka, S.: Effect of human recombinant interferon on cytotoxic activity of natural killer (NK) cells and monocytes. Cell. Immunol. 67(1), 160-167 (1982)
40. Roda, J.M., Parihar, R., Lehman, A., Mani, A., Tridandapani, S., Carson 3rd, W.E.: Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J. Immunol. 177(1), 120-129 (2006)
41. Ragupathi, G., Liu, N.X., Musselli, C., Powell, S., Lloyd, K., Livingston, P.O.: Antibodies against tumor cell glycolipids and proteins, but not mucins, mediate complement-dependent cytotoxicity. J. Immunol. 174(9), 5706-5712 (2005)
42. Juhl, H., Helmig, F., Baltzer, K., Kalthoff, H., Henne-Bruns, D., Kremer, B.: Frequent expression of complement resistance factors CD46, CD55, and CD59 on gastrointestinal cancer cells limits the therapeutic potential of monoclonal antibody 17-1A. J. Surg. Oncol. 64(3), 222-230 (1997)
43. Yu, J., Caragine, T., Chen, S., Morgan, B.P., Frey, A.B., Tomlinson, S.: Protection of human breast cancer cells from complement-mediated lysis by expression of heterologous CD59. Clin. Exp. Immunol. 115(1), 13-18 (1999)
44. Geis, N., Zell, S., Rutz, R., Li, W., Giese, T., Mamidi, S., Schultz, S., Kirschfink, M.: Inhibition of membrane complement inhibitor expression (CD46, CD55, CD59) by siRNA sensitizes tumor cells to complement attack in vitro. Curr. Cancer Drug Targets 10(8), 922-931 (2010)
45. Price, M.R., Rye, P.D., Petrakou, E., Murray, A., Brady, K., Imai, S., Haga, S., Kiyozuka, Y., Schol, D., Meulenbroek, M.F., et al.: Summary report on the ISOBM TD-4 Workshop: analysis of 56 monoclonal antibodies against the MUC1 mucin. San Diego, Calif., November 17-23, 1996. Tumour Biol. 19(Suppl 1), 1-20 (1998)
46. Courtenay-Luck, N., Pegram, M.: Phase I study of the anti-MUC-1 antibody, huHMFG1 (AS1402), in patients with advanced breast cancer. Clin. Immunol. 123, S110-S111 (2007)
47. Wahrenbrock, M.G., Varki, A.: Multiple hepatic receptors cooperate to eliminate secretory mucins aberrantly entering the bloodstream: are circulating cancer mucins the "tip of the iceberg"? Cancer Res. 66(4), 2433-2441 (2006)
48. Fan, X.N., Karsten, U., Goletz, S., Cao, Y.: Reactivity of a humanized antibody (hPankoMab) towards a tumor-related MUC1 epitope (TA-MUC1) with various human carcinomas. Pathol. Res. Pract. 206(8), 585-589 (2010)
49. Danielczyk, A., Stahn, R., Faulstich, D., Loffler, A., Marten, A., Karsten, U., Goletz, S.: PankoMab: a potent new generation anti-tumour MUC1 antibody. Cancer Immunol. Immunother. 55(11), 1337-1347 (2006)
50. Parham, P.: The genetic and evolutionary balances in human NK cell receptor diversity. Semin. Immunol. 20(6), 311-316 (2008)
51. Ferris, R.L., Jaffee, E.M., Ferrone, S.: Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J. Clin. Oncol. 28(28), 4390-4399 (2010)