Tn glycosylation of the MUC6 protein modulates its immunogenicity and promotes the induction of Th17-biased T cell responses

Journal of Biological Chemistry

Volumn 286, Issue 10, 2011, Pages 7797-7811

  Freire, Teresa ^a,b   Lo Man, Richard ^a   Bay, Sylvie ^a,b   Leclerc, Claude ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CARCINOMAS; CANCER VACCINE; CELL RESPONSE; GASTRIC TISSUE; GLYCOSYLATED; HUMAN CANCER; IMMUNOGENICITY; IMMUNOLOGICAL PROPERTIES; T CELLS; T-CELL RESPONSE; TUMOR ANTIGEN; TUMOR CELLS;

ANTIGENS; DISEASES; ESTERIFICATION; GLYCOPROTEINS; GLYCOSYLATION; MONOCLONAL ANTIBODIES; TUMORS; VACCINES;

PROTEINS;

CD4 ANTIGEN; GLYCOPROTEIN; INTERLEUKIN 17; MAJOR HISTOCOMPATIBILITY ANTIGEN; MUCIN 6; N ACETYLGALACTOSAMINE; PEPTIDE DERIVATIVE; PROTEIN DERIVATIVE; TN ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HYBRIDOMA; IMMUNOGENICITY; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; TH17 CELL; VACCINE PRODUCTION;

ANIMALS; ANTIBODIES, NEOPLASM; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; CANCER VACCINES; FEMALE; GLYCOSYLATION; HUMANS; INTERLEUKIN-17; MICE; MICE, INBRED BALB C; MUCIN-6; TH1 CELLS; TH17 CELLS; TUMOR ESCAPE;

EID: 79953155667     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M110.209742     Document Type: Article

References (69)

1. Freire, T., Bay, S., Vichier-Guerre, S., Lo-Man, R., and Leclerc, C. (2006) Mini Rev. Med. Chem. 6, 1357-1373
2. Brockhausen, I. (2006) EMBO Rep. 7, 599-604
3. Springer, G. F. (1997) J. Mol. Med. 75, 594-602
4. Hollingsworth, M. A., and Swanson, B. J. (2004) Nat. Rev. Cancer 4, 45-60
5. Gendler, S. J., and Spicer, A. P. (1995) Annu. Rev. Physiol. 57, 607-634
6. Hilkens, J., Ligtenberg, M. J., Vos, H. L., and Litvinov, S. V. (1992) Trends Biochem. Sci. 17, 359-363
7. Segal-Eiras, A., and Croce, M. V. (1997) Allergol. Immunopathol. 25, 176-181
8. Lo-Man, R., Vichier-Guerre, S., Bay, S., Dériaud, E., Cantacuzène, D., and Leclerc, C. (2001) J. Immunol. 166, 2849-2854
9. Lo-Man, R., Vichier-Guerre, S., Perraut, R., Dériaud, E., Huteau, V., Ben-Mohamed, L., Diop, O. M., Livingston, P. O., Bay, S., and Leclerc, C. (2004) Cancer Res. 64, 4987-4994
10. Reis, C. A., David, L., Carvalho, F., Mandel, U., de Bolós, C., Mirgorodskaya, E., Clausen, H., and Sobrinho-Simões, M. (2000) J. Histochem. Cytochem. 48, 377-388
11. Toribara, N. W., Roberton, A. M., Ho, S. B., Kuo, W. L., Gum, E., Hicks, J. W., Gum, J. R., Jr., Byrd, J. C., Siddiki, B., and Kim, Y. S. (1993) J. Biol. Chem. 268, 5879-5885
12. Guillem, P., Billeret, V., Buisine, M. P., Flejou, J. F., Lecomte-Houcke, M., Degand, P., Aubert, J. P., Triboulet, J. P., and Porchet, N. (2000) Int. J. Cancer 88, 856-861
13. Hamamoto, A., Abe, Y., Nishi, M., Fujimori, S., Ohnishi, Y., Yamazaki, H., Oida, Y., Miyazaki, N., Inada, K., Ueyama, Y., Iwasaki, M., Inoue, H., and Nakamura, M. (2005) Int. J. Oncol. 26, 891-896
14. Bartman, A. E., Sanderson, S. J., Ewing, S. L., Niehans, G. A., Wiehr, C. L., Evans, M. K., and Ho, S. B. (1999) Int. J. Cancer 80, 210-218
15. Pereira, M. B., Dias, A. J., Reis, C. A., and Schmitt, F. C. (2001) J. Clin. Pathol. 54, 210-213
16. Freire, T., Bay, B., von Mensdorff-Pouilly, S., and Osinaga, E. (2005) Cancer Res. 65, 7880-7887
17. Grinstead, J. S., Schuman, J. T., and Campbell, A. P. (2003) Biochemistry 42, 14293-14305
18. von Mensdorff-Pouilly, S., Kinarsky, L., Engelmann, K., Baldus, S. E., Verheijen, R. H., Hollingsworth, M. A., Pisarev, V., Sherman, S., and Hanisch, F. G. (2005) Glycobiology 15, 735-746
19. Ryan, S. O., Vlad, A. M., Islam, K., Gariépy, J., and Finn, O. J. (2009) Biol. Chem. 390, 611-618
20. Freire, T., Lo-Man, R., Piller, F., Piller, V., Leclerc, C., and Bay, S. (2006) Glycobiology 16, 390-401
21. Ten Hagen, K. G., Fritz, T. A., and Tabak, L. A. (2003) Glycobiology 13, 1R-16R
22. Freire, T., D'Alayer, J., and Bay, S. (2006) Bioconjug. Chem. 17, 559-564
23. Towbin, H., Staehelin, T., and Gordon, J. (1979) Proc. Natl. Acad. Sci. U.S.A. 76, 4350-4354
24. Lo-Man, R., Langeveld, J. P., Dériaud, E., Jehanno, M., Rojas, M., Clément, J. M., Meloen, R. H., Hofnung, M., and Leclerc, C. (2000) Infect. Immun. 68, 3079-3089
25. Gerken, T. A., Zhang, J., Levine, J., and Elhammer, A. (2002) J. Biol. Chem. 277, 49850-49862
26. Bennett, E. P., Hassan, H., Hollingsworth, M. A., and Clausen, H. (1999) FEBS Lett. 460, 226-230
27. Osinaga, E., Pancino, G., Porchet, N., Berois, N., De Cremoux, P., Mistro, D., Aubert, J. P., Calvo, F., and Roseto, A. (1994) Breast Cancer Res. Treat. 32, 139-152
28. Cloos, P. A., and Christgau, S. (2004) Biogerontology 5, 139-158
29. Pang, P. C., Tissot, B., Drobnis, E. Z., Morris, H. R., Dell, A., and Clark, G. F. (2009) J. Proteome Res. 8, 4906-4915
30. Dowling, W., Thompson, E., Badger, C., Mellquist, J. L., Garrison, A. R., Smith, J. M., Paragas, J., Hogan, R. J., and Schmaljohn, C. (2007) J. Virol. 81, 1821-1837
31. van der Burg, S. H., Visseren, M. J., Brandt, R. M., Kast, W. M., and Melief, C. J. (1996) J. Immunol. 156, 3308-3314
32. Leclerc, C., Martineau, P., Charlot, B., Delpeyroux, F., van der Werf, S., and Hofnung, M. (1997) J. Immunol. 158, 3252-3258
33. Ninkovic, T., and Hanisch, F. G. (2007) J. Immunol. 179, 2380-2388
34. Suzuki, N., Yamamoto, K., Toyoshima, S., Osawa, T., and Irimura, T. (1996) J. Immunol. 156, 128-135
35. Freire, T., Zhang, X., Dériaud, E., Ganneau, C., Vichier-Guerre, S., Azria, E., Launay, O., Lo-Man, R., Bay, S., and Leclerc, C. (2010) Blood 116, 3526-3536
36. Carbone, F. R., and Gleeson, P. A. (1997) Glycobiology 7, 725-730
37. Anderton, S. M. (2004) Curr. Opin. Immunol. 16, 753-758
38. Wei, X., Decker, J. M., Wang, S., Hui, H., Kappes, J. C., Wu, X., Salazar-Gonzalez, J. F., Salazar, M. G., Kilby, J. M., Saag, M. S., Komarova, N. L., Nowak, M. A., Hahn, B. H., Kwong, P. D., and Shaw, G. M. (2003) Nature 422, 307-312
39. Rachagani, S., Torres, M. P., Moniaux, N., and Batra, S. K. (2009) Biofactors 35, 509-527
40. Baldus, S. E., Engelmann, K., and Hanisch, F. G. (2004) Crit. Rev. Clin. Lab. Sci. 41, 189-231
41. Springer, G. F., Desai, P. R., Spencer, B. D., Tegtmeyer, H., Carlstedt, S. C., and Scanlon, E. F. (1995) Cancer Detect. Prev. 19, 374-380
42. Marcaurelle, L. A., and Bertozzi, C. R. (2002) Glycobiology 12, 69R-77R
43. Kagan, E., Ragupathi, G., Yi, S. S., Reis, C. A., Gildersleeve, J., Kahne, D., Clausen, H., Danishefsky, S. J., and Livingston, P. O. (2005) Cancer Immunol. Immunother. 54, 424-430
44. Sørensen, A. L., Reis, C. A., Tarp, M. A., Mandel, U., Ramachandran, K., Sankaranarayanan, V., Schwientek, T., Graham, R., Taylor-Papadimitriou, J., Hollingsworth, M. A., Burchell, J., and Clausen, H. (2006) Glycobiology 16, 96-107
45. George, S. K., Schwientek, T., Holm, B., Reis, C. A., Clausen, H., and Kihlberg, J. (2001) J. Am. Chem. Soc. 123, 11117-11125
46. Ajisaka, K., and Miyasato, M. (2000) Biosci. Biotechnol. Biochem. 64, 1743-1746
47. Cheng, L., Tachibana, K., Iwasaki, H., Kameyama, A., Zhang, Y., Kubota, T., Hiruma, T., Tachibana, K., Kudo, T., Guo, J. M., and Narimatsu, H. (2004) FEBS Lett. 566, 17-24
48. Schwientek, T., Bennett, E. P., Flores, C., Thacker, J., Hollmann, M., Reis, C. A., Behrens, J., Mandel, U., Keck, B., Schäfer, M. A., Haselmann, K., Zubarev, R., Roepstorff, P., Burchell, J. M., Taylor-Papadimitriou, J., Hollingsworth, M. A., and Clausen, H. (2002) J. Biol. Chem. 277, 22623-22638
49. Ten Hagen, K. G., Bedi, G. S., Tetaert, D., Kingsley, P. D., Hagen, F. K., Balys, M. M., Beres, T. M., Degand, P., and Tabak, L. A. (2001) J. Biol. Chem. 276, 17395-17404
50. Sinclair, A. M., and Elliott, S. (2005) J. Pharm. Sci. 94, 1626-1635
51. De Groot, A. S., and Scott, D. W. (2007) Trends Immunol. 28, 482-490
52. Cudic, M., Ertl, H. C., and Otvos, L., Jr. (2002) Bioorg. Med. Chem. 10, 3859-3870
53. Haurum, J. S., Arsequell, G., Lellouch, A. C., Wong, S. Y., Dwek, R. A., McMichael, A. J., and Elliott, T. (1994) J. Exp. Med. 180, 739-744
54. Mouritsen, S., Meldal, M., Christiansen-Brams, I., Elsner, H., and Werdelin, O. (1994) Eur. J. Immunol. 24, 1066-1072
55. Hermeling, S., Crommelin, D. J., Schellekens, H., and Jiskoot, W. (2004) Pharm. Res. 21, 897-903
56. Schuster, O., Klich, G., Sinnwell, V., Kränz, H., Paulsen, H., and Meyer, B. (1999) J. Biomol. NMR 14, 33-45
57. Hiltbold, E. M., Alter, M. D., Ciborowski, P., and Finn, O. J. (1999) Cell. Immunol. 194, 143-149
58. Corthay, A., Bäcklund, J., Broddefalk, J., Michaëlsson, E., Goldschmidt, T. J., Kihlberg, J., and Holmdahl, R. (1998) Eur. J. Immunol. 28, 2580-2590
59. Galli-Stampino, L., Meinjohanns, E., Frische, K., Meldal, M., Jensen, T., Werdelin, O., and Mouritsen, S. (1997) Cancer Res. 57, 3214-3222
60. Vlad, A. M., Muller, S., Cudic, M., Paulsen, H., Otvos, L., Jr., Hanisch, F. G., and Finn, O. J. (2002) J. Exp. Med. 196, 1435-1446
61. Hanisch, F. G., Schwientek, T., Von Bergwelt-Baildon, M. S., Schultze, J. L., and Finn, O. (2003) Eur. J. Immunol. 33, 3242-3254
62. Stepensky, D., Tzehoval, E., Vadai, E., and Eisenbach, L. (2006) Clin. Exp. Immunol. 143, 139-149
63. Ishioka, G. Y., Lamont, A. G., Thomson, D., Bulbow, N., Gaeta, F. C., Sette, A., and Grey, H. M. (1992) J. Immunol. 148, 2446-2451
64. Harding, C. V., Kihlberg, J., Elofsson, M., Magnusson, G., and Unanue, E. R. (1993) J. Immunol. 151, 2419-2425
65. Denda-Nagai, K., Aida, S., Saba, K., Suzuki, K., Moriyama, S., Oo-Puthinan, S., Tsuiji, M., Morikawa, A., Kumamoto, Y., Sugiura, D., Kudo, A., Akimoto, Y., Kawakami, H., Bovin, N. V., and Irimura, T. (2010) J. Biol. Chem. 285, 19193-19204
66. Kryczek, I., Banerjee, M., Cheng, P., Vatan, L., Szeliga, W., Wei, S., Huang, E., Finlayson, E., Simeone, D., Welling, T. H., Chang, A., Coukos, G., Liu, R., and Zou, W. (2009) Blood 114, 1141-1149
67. Kryczek, I., Wei, S., Zou, L., Altuwaijri, S., Szeliga, W., Kolls, J., Chang, A., and Zou, W. (2007) J. Immunol. 178, 6730-6733
68. Martin-Orozco, N., Muranski, P., Chung, Y., Yang, X. O., Yamazaki, T., Lu, S., Hwu, P., Restifo, N. P., Overwijk, W. W., and Dong, C. (2009) Immunity 31, 787-798
69. Leibundgut-Landmann, S., Osorio, F., Brown, G. D., and Reis e Sousa, C. (2008) Blood 112, 4971-4980