Site-specific conformational alteration induced by sialylation of MUC1 tandem repeating glycopeptides at an epitope region for the anti-KL-6 monoclonal antibody

Biochemistry

Volumn 52, Issue 2, 2013, Pages 402-414

  Matsushita, Takahiko ^a   Ohyabu, Naoki ^a   Fujitani, Naoki ^a   Naruchi, Kentaro ^b   Shimizu, Hiroki ^c   Hinou, Hiroshi ^a,b   Nishimura, Shin Ichiro ^a,b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b Hokkaido University and Medicinal Chemistry Pharmaceuticals LLC   (Japan)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FUNCTIONS; CONFORMATIONAL CHANGE; CONTROLLING STRUCTURE; GLYCOPEPTIDES; HUMAN EPITHELIAL CELLS; IMMUNE RESPONSE; MUC1 GLYCOPROTEIN; O-GLYCANS; O-GLYCOSYLATION; SEQUENCE-DEPENDENT; SIALYLATION; SITE-SPECIFIC; STRUCTURAL ALTERATIONS; STRUCTURAL CHARACTERIZATION; TANDEM REPEATS; TUMORIGENESIS;

ANTIGENS; CELL ADHESION; CELL MEMBRANES; CONFORMATIONS; ESTERIFICATION; GLYCOPROTEINS; MONOCLONAL ANTIBODIES; PATHOLOGY; PEPTIDES;

GLYCOSYLATION;

ALANINE; ARGININE; ASPARTIC ACID; EPITOPE; GLYCAN; GLYCINE; HISTIDINE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY KL 6; MUCIN 1; PROLINE; SERINE; THREONINE; UNCLASSIFIED DRUG; VALINE;

AMINO ACID SEQUENCE; ANTIGEN RECOGNITION; ANTIGEN STRUCTURE; ARTICLE; CELL SURFACE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE BINDING SITE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; SIALYLATION; STRUCTURE ANALYSIS; VARIABLE NUMBER OF TANDEM REPEAT;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; EPITOPES; GLYCOSYLATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUCIN-1; N-ACETYLNEURAMINIC ACID; NEOPLASMS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN CONFORMATION;

EID: 84872546499     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3013142     Document Type: Article

References (77)

1. Brockhausen, I. (1999) Pathways of O -glycan biosynthesis in cancer cells Biochim. Biophys. Acta 1473, 67-95
2. Taylor-Papadimitriou, J. (1999) MUC1 and cancer Biochim. Biophys. Acta 1455, 301-313
3. Rosen, S. D. (2004) Ligands for L-selectin: Homing, inflammation, and beyond Annu. Rev. Immunol. 22, 129-156
4. Rose, M. C. and Voynow, J. A. (2006) Respiratory tract mucin genes and mucin glycoproteins in health and disease Physiol. Rev. 86, 245-278
5. Hollingsworth, M. A. and Swanson, B. J. (2004) Mucins in cancer: Protection and control of the cell surface Nat. Rev. Cancer 4, 45-60
6. Ludwig, J. A. and Weinstein, J. N. (2005) Biomarkers in cancer staging, prognosis and treatment selection Nat. Rev. Cancer 5, 845-856
7. Dube, D. H. and Bertozzi, C. R. (2005) Glycans in cancer and inflammation. Potential for therapeutics and diagnostics Nat. Rev. Drug Discovery 4, 477-488
8. Tachibana, Y., Fletcher, G. L., Fujitani, N., Tsuda, S., Monde, K., and Nishimura, S.-I. (2004) Antifreeze glycoproteins: Elucidation of the structural motifs that are essential for antifreeze activity Angew. Chem., Int. Ed. 43, 856-862
9. Ohyabu, N., Hinou, H., Matsushita, T., Izumi, R., Shimizu, H., Kawamoto, K., Numata, Y., Togame, H., Takemoto, H., Kondo, H., and Nishimura, S.-I. (2009) An Essential Epitope of Anti-MUC1 Monoclonal Antibody KL-6 Revealed by Focused Glycopeptide Library J. Am. Chem. Soc. 131, 17102-17109
10. Hashimoto, R., Fujitani, N., Takegawa, Y., Kurogochi, M., Matsushita, T., Naruchi, K., Ohyabu, N., Hinou, H., Gao, X.-D., Manri, N., Satake, H., Kaneko, A., Sakamoto, T., and Nishimura, S.-I. (2011) An Efficient Approach for the Characterization of Mucin-Type Glycopeptides: The Effect of O -Glycosylation on the Conformation of Synthetic Mucin Peptides Chem.-Eur. J. 17, 2393-2404
11. Shimizu, K. H., Hosoguchi, K., Liu, Y., Fujitani, N., Ohta, T., Hinou, H., Matsushita, T., Shimizu, H., Feizi, T., and Nishimura, S.-I. (2010) Chemical Synthesis, Folding, and Structural Insights into O -Fucosylated Epidermal Growth Factor-like Repeat 12 of Mouse Notch-1 Receptor J. Am. Chem. Soc. 132, 14857-14865
12. Coltart, D. M., Royyuru, A. K., Williams, L. J., Glunz, P. W., Sames, D., Kuduk, S. D., Schwarz, J. B., Chen, X.-T., Danishefsky, S. J., and Live, D. H. (2002) Principles of mucin architecture: Structural studies on synthetic glycopeptides bearing clustered mono-, di-, tri-, and hexasaccharide glycodomains J. Am. Chem. Soc. 124, 9833-9844
13. Corzana, F., Busto, J. H., Osés, G. J., Asensio, J. L., Barbero, J. J., Peregrina, J. M., and Avenoza, A. (2006) New insights into α-GalNAc-Ser motif: Influence of hydrogen bonding versus solvent interactions on the preferred conformation J. Am. Chem. Soc. 128, 14640-14684
14. Corzana, F., Busto, J., Engelsen, S. B., Barbero, J. J., Asensio, J. L., Peregrina, J. M., and Avenoza, A. (2006) Effect of β- O -glucosylation on l -Ser and l -Thr diamides: A bias toward α-helical conformations Chem.-Eur. J. 12, 7864-7871
15. Corzana, F., Busto, J. H., Osés, G. J., de Luis, M. G., Asensio, J. L., Barbero, J. J., Peregrina, J. M., and Avenoza, A. (2007) Serine versus threonine glycosylation: The methyl group causes a drastic alteration on the carbohydrate orientation and on the surrounding water shell J. Am. Chem. Soc. 129, 9458-9467
16. Corzana, F., Busto, J. H., de Luis, M. G., Barbero, J. J., and Avenoza, A. (2009) The Nature and Sequence of the Amino Acid Aglycone Strongly Modulates the Conformation and Dynamics Effects of Tn Antigen's Clusters Chem.-Eur. J. 15, 3863-3874
17. Live, D. H., Williams, L. J., Kuduk, S. D., Schwarz, J. B., Glunz, P. W., Chen, X.-T., Sames, D., Kumar, R. A., and Danishefsky, S. J. (1999) Probing cell-surface architecture through synthesis: An NMR-determined structural motif for tumor-associated mucins Proc. Natl. Acad. Sci. U.S.A. 96, 3489-3493
18. Kirnarsky, L., Prakash, O., Vogen, S. M., Nomoto, M., Hollingsworth, M. A., and Sherman, S. (2000) Structural effects of O -glycosylation on a 15-residue peptide from the mucin (MUC1) core protein Biochemistry 39, 12076-12082
19. Wormald, M. R., Petrescu, A. J., Pao, Y. L., Glithero, A., Elliott, T., and Dwek, R. A. (2002) Conformational studies of oligosaccharides and glycopeptides: Complementarity of NMR, X-ray crystallography, and molecular modelling Chem. Rev. 102, 371-386
20. Kinarsky, L., Suryanarayanan, G., Prakash, O., Paulsen, H., Clausen, H., Hanisch, F.-G., Hollingsworth, M. A., and Sherman, S. (2003) Conformational studies on the MUC1 tandem repeat glycopeptides: Implication for the enzymatic O -glycosylation of the mucin protein core Glycobiology 13, 929-939
21. Jinek, M., Chen, Y.-W., Clausen, H., Cohen, S. M., and Conti, E. (2006) Structural insights into the Notch-modifying glycosyltransferase Fringe Nat. Struct. Mol. Biol. 13, 945-946
22. Kuhn, A. and Kunz, H. (2007) Saccharide-induced peptide conformation in glycopeptides of the recognition region of LI-cadherin Angew. Chem., Int. Ed. 46, 454-458
23. Ten Hagen, K. G., Fritz, T. A., and Tabak, L. A. (2003) All in the family: The UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases Glycobiology 13, 1-16
24. Ju, T., Otto, V. I., and Cummings, R. D. (2011) The Tn Antigen-Structural Simplicity and Biological Complexity Angew. Chem., Int. Ed. 50, 1770-1791
25. Borgert, A., Heimburg-Molinaro, J., Song, X., Lasanajak, Y., Ju, T., Liu, M., Thompson, P., Ragpathi, G., Barany, U., Smith, D. F., Cummings, R. D., and Live, D. (2012) Deciphering structural elements of mucin glycoprotein recognition ACS Chem. Biol. 7, 1031-1039
26. Prince, M. R., Rye, P. D., Petrakou, E., Murray, A., Brady, K., Imai, S., Haga, S., Kiyozuka, Y., Schol, D., Meulenbroek, M. F., Snijdewint, F. G., von Mensdorff-Pouilly, S., Verstraeten, R. A., Kenemans, P., Blockzjil, A., Nilsson, K., Nilsson, O., Reddish, M., Suresh, M. R., Koganty, R. R., Forter, S., Baronic, L., Berg, A., Longenecker, M. B., and Higers, J. (1998) Summary Report on the ISOBM TD-4 Workshop: Analysis of 56 Monoclonal Antibodies against the MUC1Mucin Tumor Biol. 19, 1-20
27. Hattrup, C. L. and Gendler, S. J. (2008) Structure and function of the cell surface (tethered) mucins Annu. Rev. Physiol. 70, 431-457
28. Tarp, M. A. and Clausen, H. (2009) Mucin-type O -glycosylation and its potential use in drug and vaccine development Biochim. Biophys. Acta 1780, 546-563
29. Springer, G. F. (1984) T and TN, general carcinoma auto-antigens Science 224, 1198-1206
30. Taylor-Papadimitriou, J. and Epenetos, A. A. (1994) Exploiting altered glycosylation patterns in cancer: Progress and challenges in diagnosis and therapy Trends Biotechnol. 12, 227-233
31. Lloyd, K. O., Burchell, J., Kudryashov, V., Yin, B. W. T., and 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
32. Brockhausen, I. (1999) Pathways of O -glycan biosynthesis in cancer cells Biochim. Biophys. Acta 1473, 67-95
33. Burchell, J. M., Mungul, A., and Taylor-Papadimitriou, J. (2001) O -linked glycosylation in the mammary gland: Changes that occur during malignancy Journal of Mammary Gland Biology and Neoplasia 6, 355-363
34. Hanisch, F.-G., Standie, T., and Bosslet, K. (1995) Monoclonal-antibody BW835 defines a site-specific Thomsen-Friedenreich disaccharide linked to threonine within the VTSA motif of MUC1 tandem repeats Cancer Res. 55, 4036-4040
35. Dai, J., Allard, W. J., Davis, G., and Yeung, K. K. (1998) Effect of desialylation on binding, affinity, and specificity of 56 monoclonal antibodies against MUC1 mucin Tumor Biol. 19, 100-110
36. Grinstead, J. S., Koganty, R. R., Krantz, M. J., Longencker, B. M., and Campbell, A. P. (2002) Effect of glycosylation on MUC1 humoral immune recognition: NMR studies of MUC1 glycopeptide-antibody interactions Biochemistry 41, 9946-9961
37. Takeuchi, H., Kato, K., da-Nagai, K., Hanisch, F. G., Clausen, H., and Irimura, T. (2002) The epitope recognized by the unique anti-MUC1 monoclonal antibody MY.1E12 involves sialyl α2-3galactosyl β1-3N- acetylgalactosaminide linked to a distinct threonine residue in the MUC1 tandem repeat J. Immunol. Methods 270, 199-209
38. Grinstead, J. S., Schuman, J. T., and Campbell, A. P. (2003) Epitope mapping of antigenic MUC1 peptides to breast cancer antibody fragment B27.29: A heteronuclear NMR study Biochemistry 42, 14293-14305
39. Danielczyk, A., Stahn, R., Faulstich, D., Löffler, A., Märten, A., Karsten, U., and Goletz, S. (2006) PankoMab: A potent new generation anti-tumour MUC1 antibody Cancer Immunol. Immunother. 55, 1337-1347
40. Tarp, M. A., Sørensen, A. L., Mandel, U., Paulsen, H., Burchell, G. M., Taylor-Papadimitriou, J., and Clausen, H. (2007) Identification of a novel cancer-specific immunodominant glycopeptide epitope in the MUC1 tandem repeat Glycobiology 17, 197-209
41. Müller, S., Goletz, S., Packer, N., Gooley, A., Lawson, A. M., and Hanisch, F.-G. (1997) Localization of O -glycosylation sites on glycopeptide fragments from lactation-associated MUC1: All putative sites within the tandem repeat are glycosylation targets in vivo J. Biol. Chem. 272, 24780-24793
42. Müller, S. and Hanisch, F.-G. (2002) Recombinant MUC1 probe authentically reflects cell-specific O -glycosylation profiles of endogenous breast cancer mucin: High density and prevalent core 2-based glycosylation J. Biol. Chem. 277, 26103-26112
43. Kohno, N., Akiyama, M., Kyoizumi, S., Hakoda, M., Kobuke, K., and Yamakido, M. (1988) Detection of soluble tumor-associated antigens in sera and effusions using novel monoclonal antibodies, KL-3 and KL-6, against lung adenocarcinoma Jpn. J. Clin. Oncol. 18, 203-216
44. Ogawa, Y., Ishikawa, T., Ikeda, K., Nakada, B., Sawada, T., Ogisawa, K., Kato, Y., and Hirasawa, K. (2000) Evaluation of serum KL-6, a mucin-like glycoprotein, as a tumor marker for breast cancer Clin. Cancer Res. 6, 4069-4072
45. Hirasawa, Y., Kohno, N., Yokoyama, A., Kondo, K., Hiwada, K., and Miyake, M. (2000) Natural autoantibody to MUC1 is a prognostic indicator for non-small cell lung cancer Am. J. Respir. Crit. Care Med. 161, 589-594
46. Kurosaki, M., Izumi, N., Onuki, Y., Nishimura, Y., Ueda, K., Tsuchiya, K., Nakanishi, H., Kitamura, T., Asahina, Y., Uchihara, M., and Miyake, S. (2005) Serum KL-6 as a novel tumor marker for hepatocellular carcinoma in hepatitis C virus infected patients Hepatol. Res. 33, 250-257
47. Amal, G., Tanaka, E., Matsumoto, A., Abd-el Wahab, M., Serwah, el-H., Attia, F., Ali, K., Hassouba, H., el-Deeb, A. el-R., Ichijo, T., Umemura, T., Huto, H., Yoshizawa, K., and Kiyosawa, K. (2005) Assessment of KL-6 as a tumor marker in patients with hepatocellular carcinoma World J. Gastroenterol. 11, 6607-6612
48. Guo, Q., Tang, W., Inagaki, Y., Midorikawa, Y., Kokudo, N., Sugawara, Y., Nakata, M., Konishi, T., Nagawa, H., and Makuuchi, M. (2006) Clinical significance of subcellular localization of KL-6 mucin in primary colorectal adenocarcinoma and metastatic tissues World J. Gastroenterol. 12, 54-59
49. Inata, J., Hattori, N., Yokoyama, A., Ohshiro, S., Doi, M., Ishikawa, N., Hamada, H., and Kohno, N. (2007) Circulating KL-6/MUC1 mucin carrying sialyl Lewis(a) oligosaccharide is an independent prognostic factor in patients with lung adenocarcinoma Int. J. Cancer 120, 2643-2649
50. Ishikawa, N., Hattori, N., Yokoyama, A., Tanaka, S., Nishino, R., Yoshikawa, K., Ohshimo, S., Fujitaka, K., Ohnishi, H., Hamada, H., Arihiro, K., and Kohno, N. (2008) Usefulness of monitoring the circulating Krebs von den Lungen-6 levels to predict the clinical outcome of patients with advanced nonsmall cell lung cancer treated with epidermal growth factor receptor tyrosine kinase inhibitors Int. J. Cancer 122, 2612-2620
51. Miura, Y., Kato, K., Takegawa, Y., Kurogochi, M., Furukawa, J., Shinohara, Y., Nagahori, N., Amano, M., Hinou, H., and Nishimura, S.-I. (2010) Glycoblotting-Assisted O -Glycomics: Ammonium Carbamate Allows for Highly Efficient O -Glycan Release from Glycoproteins Anal. Chem. 82, 10021-10029
52. Matsushita, T., Hinou, H., Kurogochi, M., Shimizu, H., and Nishimura, S.-I. (2005) Rapid microwave-assisted solid-phase glycopeptide synthesis Org. Lett. 7, 877-880
53. Bothner-By, A. A., Stephens, R. L., Lee, J.-M., Warren, C. D., and Jeanloz, R. W. (1984) Structure determination of a tetrasaccharide: Transient nuclear Overhauser effects in the rotating frame J. Am. Chem. Soc. 106, 811-813
54. Bax, A. and Davis, D. G. (1985) Practical aspects of two-dimensional transverse NOE spectroscopy J. Magn. Reson. 63, 207-213
55. Piotto, M., Saudek, V., and Sklenár, V. (1992) Gradient-tailored excitation for single-quantum NMR-spectroscopy of aqueous-solutions J. Biomol. NMR 2, 661-665
56. Delaglio, F., Grzesiek, S., Vuister, G., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPIPE: A multidimensional spectral processing system based on UNIX PIPES J. Biomol. NMR 6, 277-293
57. Goddard, T. D. and Kneller, D. G. (2008) SPARKY 3, University of California, San Francisco.
58. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D54, 905-921
59. Laskowski, R. A., Rullmann, J. A. C., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8, 477-486
60. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures J. Mol. Graphics 14, 51-55
61. Fumoto, M., Hinou, H., Matsushita, T., Kurogochi, M., Ohta, T., Ito, T., Yamada, K., Takimoto, A., Kondo, H., Inazu, T., and Nishimura, S.-I. (2005) Molecular transporter between polymer platforms: Highly efficient chemoenzymatic glycopeptide synthesis by the combined use of solid-phase and water-soluble polymer supports Angew. Chem., Int. Ed. 44, 2534-2537
62. Fumoto, M., Hinou, H., Ohta, T., Ito, T., Yamada, K., Takimoto, A., Kondo, H., Shimizu, H., Inazu, T., Nakahara, Y., and Nishimura, S.-I. (2005) Combinatorial synthesis of MUC1 glycopeptides: Polymer blotting facilitates chemical and enzymatic synthesis of highly complicated mucin glycopeptides J. Am. Chem. Soc. 127, 11804-11818
63. Matsushita, T., Hinou, H., Fumoto, M., Kurogochi, M., Fujitani, N., Shimizu, H., and Nishimura, S.-I. (2006) Construction of highly glycosylated mucin-type glycopeptides based on microwave-assisted solid-phase syntheses and enzymatic modifications J. Org. Chem. 71, 3051-3063
64. Naruchi, K., Hamamoto, T., Kurogochi, M., Hinou, H., Shimizu, H., Matsushita, T., Fujitani, N., Kondo, H., and Nishimura, S.-I. (2006) Construction and structural characterization of versatile lactosaminoglycan- related compound library for the synthesis of complex glycopeptides and glycosphingolipids J. Org. Chem. 71, 9609-9621
65. Matsushita, T., Sadamoto, R., Ohyabu, N., Nakata, H., Fumoto, H., Fujitani, N., Takegawa, Y., Sakamoto, T., Kurogochi, M., Hinou, H., Shimizu, H., Ito, T., Naruchi, K., Togame, H., Takemoto, H., Kondo, H., and Nishimura, S.-I. (2009) Functional Neoglycopeptides: Synthesis and Characterization of a New Class of MUC1 Glycoprotein Models Having Core 2-Based O -Glycan and Complex-Type N-Glycan Chains Biochemistry 48, 11117-11133
66. Matsushita, T., Nagashima, I., Fumoto, M., Ohta, T., Yamada, K., Shimizu, H., Hinou, H., Naruchi, K., Ito, T., Kondo, H., and Nishimura, S.-I. (2010) Artificial Golgi Apparatus: Globular Protein-like Dendrimer Facilitates Fully Automated Enzymatic Glycan Synthesis J. Am. Chem. Soc. 132, 16651-16656
67. Naruchi, K. and Nishimura, S.-I. (2011) Membrane-Bound Stable Glycosyltransferases: Highly Oriented Protein Immobilization by a C-Terminal Cationic Amphipathic Peptide Angew. Chem., Int. Ed. 80, 1328-1331
68. Meinjohannes, E., Meldal, M., Schleyer, A., Paulsen, H., and Bock, K. (1996) Efficient syntheses of core 1, core 2, core 3 and core 4 building blocks for SPS of mucin O -glycopeptides based on the N-Dts-method J. Chem. Soc., Perkin Trans. 1 985-993
69. Mathieux, N., Paulsen, H., Meldal, M., and Bock, B. (1997) Synthesis of glycopeptide sequences of repeating units of the mucins MUC 2 and MUC 3 containing oligosaccharide side-chains with core 1, core 2, core 3, core 4 and core 6 structure J. Chem. Soc., Perkin Trans. 1 2359-2368
70. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley and Sons, New York.
71. Grinstead, J. S., Koganty, R. R., Krantz, M. J., Longencker, B. M., and Campbell, A. P. (2002) Effect of glycosylation on MUC1 humoral immune recognition: NMR studies of MUC1 glycopeptide-antibody interactions Biochemistry 41, 9946-9961
72. Milner-White, E. J., Ross, B. M., Ismail, R., Belhadj-Mostefa, K., and Poet, R. (1988) One type of γ-turn, rather than the other gives rise to chain-reversal in proteins J. Mol. Biol. 204, 777-782
73. Lewis, P. N., Momany, F. A., and Scheraga, H. A. (1973) Chain reversals in proteins Biochim. Biophys. Acta 303, 211-229
74. Wüthrich, K., Billeter, M., and Braun, W. (1984) Polypeptide secondary structure determination by nuclear magnetic-resonance observation of short proton proton distances J. Mol. Biol. 180, 715-740
75. Connolly, M. L. (1983) Analytical molecular-surface calculation J. Appl. Crystallogr. 16, 548-558
76. Dziadek, S., Griesinger, C., Kunz, H., and Reinscheid, U. M. (2006) Synthesis and structural model of an α(2,6)-sialyl-T glycosylated MUC1 eicosapeptide under physiological conditions Chem.-Eur. J. 12, 4981-4993
77. Tsuboi, S., Sutoh, M., Hatakeyama, S., Hiraoka, N., Habuchi, T., Horikawa, Y., Hashimoto, Y., Yoneyama, T., Mori, K., Koie, T., Nakamura, T., Saitoh, H., Yamaya, K., Funyu, T., Fukuda, M., and Ohyama, C. (2011) A novel strategy for evasion of NK cell immunity by tumours expressing core 2 O -glycans EMBO J. 30, 3173-3185