The absence of core fucose up-regulates gnt-iii and wnt target genes: A possible mechanism for an adaptive response in terms of glycan function

Journal of Biological Chemistry

Volumn 289, Issue 17, 2014, Pages 11704-11714

  Kurimoto, Ayako ^a   Kitazume, Shinobu ^a   Kizuka, Yasuhiko ^a   Nakajima, Kazuki ^a   Oka, Ritsuko ^a   Fujinawa, Reiko ^a   Korekane, Hiroaki ^a   Yamaguchi, Yoshiki ^a   Wada, Yoshinao ^b   Taniguchi, Naoyuki ^a  

^a RIKEN   (Japan)

^b RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION;

ADAPTIVE REGULATION; ADAPTIVE RESPONSE; BIOSYNTHETIC ENZYMES; ENHANCED GENE EXPRESSION; POSSIBLE MECHANISMS; TARGET GENES; UP-REGULATION; WNT SIGNALING PATHWAYS;

POLYSACCHARIDES;

ALPHA 1,6 FUCOSE; BETA CATENIN; BETA1 INTEGRIN; FUCOSE; GLYCAN; IMMUNOGLOBULIN G; MESSENGER RNA; N ACETYLGLUCOSAMINYLTRANSFERASE; N ACETYLGLUCOSAMINYLTRANSFERASE III; NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; FIBROBLAST; FUCOSYLATION; GENE EXPRESSION; GENE TARGETING; GLYCOSYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIALYLATION; STRUCTURE ANALYSIS; UPREGULATION;

BETA-CATENIN; BISECTING GLCNAC; CORE FUCOSE; FUT8; GLYCOSYLTRANSFERASES; GNT-III; LECTIN; MASS SPECTROMETRY (MS); OXIDATIVE STRESS; WNT PATHWAY;

ANIMALS; CELLS, CULTURED; FUCOSE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; N-ACETYLGLUCOSAMINYLTRANSFERASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYSACCHARIDES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; UP-REGULATION; WNT PROTEINS;

EID: 84899427302     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.502542     Document Type: Article

References (48)

1. Orr, S. L., Le, D., Long, J. M., Sobieszczuk, P., Ma, B., Tian, H., Fang, X., Paulson, J. C., Marth, J. D., and Varki, N. (2013) A phenotype survey of 36 mutant mouse strains with gene-targeted defects in glycosyltransferases or glycan-binding proteins. Glycobiology 23, 363-380
2. Wilson, J. R., Williams, D., and Schachter, H. (1976) The control of glycoprotein synthesis: N-acetylglucosamine linkage to a mannose residue as a signal for the attachment of L-fucose to the asparagine-linked N-acetylglucosamine residue of glycopeptide from α1-acid glycoprotein. Biochem. Biophys. Res. Commun. 72, 909-916
3. Uozumi, N., Yanagidani, S., Miyoshi, E., Ihara, Y., Sakuma, T., Gao, C. X., Teshima, T., Fujii, S., Shiba, T., and Taniguchi, N. (1996) Purification and cDNA cloning of porcine brain GDP-L-Fuc:N-acetyl-β-D-glucosaminide α1→6fucosyltransferase. J. Biol. Chem. 271, 27810-27817
4. Yanagidani, S., Uozumi, N., Ihara, Y., Miyoshi, E., Yamaguchi, N., and Taniguchi, N. (1997) Purification and cDNA cloning of GDP-L-Fuc:Nacetyl- β-D-glucosaminide:α1-6 fucosyltransferase (α1-6 FucT) from human gastric cancer MKN45 cells. J. Biochem. 121, 626-632
5. Wang, X., Inoue, S., Gu, J., Miyoshi, E., Noda, K., Li, W., Mizuno- Horikawa, Y., Nakano, M., Asahi, M., Takahashi, M., Uozumi, N., Ihara, S., Lee, S. H., Ikeda, Y., Yamaguchi, Y., Aze, Y., Tomiyama, Y., Fujii, J., Suzuki, K., Kondo, A., Shapiro, S. D., Lopez-Otin, C., Kuwaki, T., Okabe, M., Honke, K., and Taniguchi, N. (2005) Dysregulation of TGF-β1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 102, 15791-15796
6. Wang, X., Gu, J., Ihara, H., Miyoshi, E., Honke, K., and Taniguchi, N. (2006) Core fucosylation regulates epidermal growth factor receptor-mediated intracellular signaling. J. Biol. Chem. 281, 2572-2577
7. Wang, X., Gu, J., Miyoshi, E., Honke, K., and Taniguchi, N. (2006) Phenotype changes of Fut8 knockout mouse: core fucosylation is crucial for the function of growth factor receptor(s). Methods Enzymol. 417, 11-22
8. Shinkawa, T., Nakamura, K., Yamane, N., Shoji-Hosaka, E., Kanda, Y., Sakurada, M., Uchida, K., Anazawa, H., Satoh, M., Yamasaki, M., Hanai, N., and Shitara, K. (2003) The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem. 278, 3466-3473
9. Matsumiya, S., Yamaguchi, Y., Saito, J., Nagano, M., Sasakawa, H., Otaki, S., Satoh, M., Shitara, K., and Kato, K. (2007) Structural comparison of fucosylated and nonfucosylated Fc fragments of human immunoglobulin G1. J. Mol. Biol. 368, 767-779
10. Umaña, P., Jean-Mairet, J., Moudry, R., Amstutz, H., and Bailey, J. E. (1999) Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody- dependent cellular cytotoxic activity. Nat. Biotechnol. 17, 176-180
11. Hodoniczky, J., Zheng, Y. Z., and James, D. C. (2005) Control of recombinant monoclonal antibody effector functions by Fc N-glycan remodeling in vitro. Biotechnol. Prog. 21, 1644-1652
12. Xu, Q., Isaji, T., Lu, Y., Gu, W., Kondo, M., Fukuda, T., Du, Y., and Gu, J. (2012) Roles of N-acetylglucosaminyltransferase III in epithelial-to- mesenchymal transition induced by transforming growth factor β1 (TGF-β1) in epithelial cell lines. J. Biol. Chem. 287, 16563-16574
13. Kitada, T., Miyoshi, E., Noda, K., Higashiyama, S., Ihara, H., Matsuura, N., Hayashi, N., Kawata, S., Matsuzawa, Y., and Taniguchi, N. (2001) The addition of bisecting N-acetylglucosamine residues to E-cadherin downregulates the tyrosine phosphorylation of β-catenin. J. Biol. Chem. 276, 475-480
14. Shigeta, M., Shibukawa, Y., Ihara, H., Miyoshi, E., Taniguchi, N., and Gu, J. (2006) β1,4-N-Acetylglucosaminyltransferase III potentiates β1 integrinmediated neuritogenesis induced by serum deprivation in Neuro2a cells. Glycobiology 16, 564-571
15. Yoshimura, M., Ihara, Y., Matsuzawa, Y., and Taniguchi, N. (1996) Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J. Biol. Chem. 271, 13811-13815
16. Pinho, S. S., Figueiredo, J., Cabral, J., Carvalho, S., Dourado, J., Magalhães, A., Gärtner, F., Mendonfa, A. M., Isaji, T., Gu, J., Carneiro, F., Seruca, R., Taniguchi, N., and Reis, C. A. (2013) E-cadherin and adherens-junctions stability in gastric carcinoma: Functional implications of glycosyltransferases involvingN-glycan branching biosynthesis,N- acetylglucosaminyltransferases III and V. Biochim. Biophys. Acta 1830, 2690-2700
17. Pinho, S. S., Reis, C. A., Paredes, J., Magalhães, A. M., Ferreira, A. C., Figueiredo, J., Xiaogang, W., Carneiro, F., Gärtner, F., and Seruca, R. (2009) The role of N-acetylglucosaminyltransferase III and V in the post-transcriptional modifications of E-cadherin. Hum. Mol. Genet. 18, 2599-2608
18. Takahashi, M., Kuroki, Y., Ohtsubo, K., and Taniguchi, N. (2009) Core fucose and bisecting GlcNAc, the direct modifiers of the N-glycan core: their functions and target proteins. Carbohydr. Res. 344, 1387-1390
19. Taniguchi, N., Miyoshi, E., Gu, J., Jianguo, G., Honke, K., and Matsumoto, A. (2006) Decoding sugar functions by identifying target glycoproteins. Curr. Opin. Struct. Biol. 16, 561-566
20. Taniguchi, N., Yoshimura, M., Miyoshi, E., Ihara, Y., Nishikawa, A., and Fujii, S. (1996) Remodeling of cell surface glycoproteins by N-acetylglucosaminyltransferase III gene transfection: Modulation of metastatic potentials and down regulation of hepatitis B virus replication. Glycobiology 6, 691-694
21. Santer, U. V., and Glick, M. C. (1979) Partial structure of a membrane glycopeptide from virus-transformed hamster cells. Biochemistry 18, 2533-2540
22. Longmore, G. D., and Schachter, H. (1982) Product-identification and substrate-specificity studies of the GDP-L-fucose:2-acetamido-2-deoxy- β-D-glucoside (FUC goes to Asn-linked GlcNAc) 6-α-L- fucosyltransferase in a Golgi-rich fraction from porcine liver. Carbohydr. Res. 100, 365-392
23. Nishima, W., Miyashita, N., Yamaguchi, Y., Sugita, Y., and Re, S. (2012) Effect of bisecting GlcNAc and core fucosylation on conformational properties of biantennary complex-type N-glycans in solution. J. Phys. Chem. B 116, 8504-8512
24. Korekane, H., Matsumoto, A., Ota, F., Hasegawa, T., Misonou, Y., Shida, K., Miyamoto, Y., and Taniguchi, N. (2010) Involvement of ST6Gal I in the biosynthesis of a unique human colon cancer biomarker candidate, β2,6- sialylated blood group type 2H (ST2H) antigen. J. Biochem. 148, 359-370
25. Nishikawa, A., Gu, J., Fujii, S., and Taniguchi, N. (1990) Determination of N-acetylglucosaminyltransferases III, IV and V in normal and hepatoma tissues of rats. Biochim. Biophys. Acta 1035, 313-318
26. Hodge, J. E., and Hofreiter, B. T. (1962) Determination of reducing sugars and carbohydrates in Methods Carbohydr. Chem. (Whistler, R. L. and Wolfrom, J. L., eds) Vol. 1, pp. 380-394, Academic Press, New York
27. Ito, H., Kuno, A., Sawaki, H., Sogabe, M., Ozaki, H., Tanaka, Y., Mizokami, M., Shoda, J., Angata, T., Sato, T., Hirabayashi, J., Ikehara, Y., and Narimatsu, H. (2009) Strategy for glycoproteomics: identification of glycoalteration using multiple glycan profiling tools. J. Proteome Res. 8, 1358-1367
28. Domon, B., and Costello, C. E. (1988) Structure elucidation of glycosphingolipids and gangliosides using high-performance tandem mass spectrometry. Biochemistry 27, 1534-1543
29. Wada, Y., Tajiri, M., and Ohshima, S. (2010) Quantitation of saccharide compositions of O-glycans by mass spectrometry of glycopeptides and its application to rheumatoid arthritis. J. Proteome Res. 9, 1367-1373
30. Wada, Y., Tajiri, M., and Yoshida, S. (2004) Hydrophilic affinity isolation and MALDI multiple-stage tandem mass spectrometry of glycopeptides for glycoproteomics. Anal. Chem. 76, 6560-6565
31. Wada, Y., Azadi, P., Costello, C. E., Dell, A., Dwek, R. A., Geyer, H., Geyer, R., Kakehi, K., Karlsson, N. G., Kato, K., Kawasaki, N., Khoo, K. H., Kim, S., Kondo, A., Lattova, E., Mechref, Y., Miyoshi, E., Nakamura, K., Narimatsu, H., Novotny, M. V., Packer, N. H., Perreault, H., Peter-Katalinic, J., Pohlentz, G., Reinhold, V. N., Rudd, P. M., Suzuki, A., and Taniguchi, N. (2007) Comparison of the methods for profiling glycoprotein glycans- HUPO Human Disease Glycomics/Proteome Initiative multi-institutional study. Glycobiology 17, 411-422
32. Matsumura, K., Higashida, K., Ishida, H., Hata, Y., Yamamoto, K., Shigeta, M., Mizuno-Horikawa, Y., Wang, X., Miyoshi, E., Gu, J., and Taniguchi, N. (2007) Carbohydrate binding specificity of a fucose-specific lectin from Aspergillus oryzae: a novel probe for core fucose. J. Biol. Chem. 282, 15700-15708
33. Zhao, Y., Nakagawa, T., Itoh, S., Inamori, K., Isaji, T., Kariya, Y., Kondo, A., Miyoshi, E., Miyazaki, K., Kawasaki, N., Taniguchi, N., and Gu, J. (2006) N-Acetylglucosaminyltransferase III antagonizes the effect of N-acetylglucosaminyltransferase V on α3β1 integrin-mediated cell migration. J. Biol. Chem. 281, 32122-32130
34. Ashline, D. J., Lapadula, A. J., Liu, Y. H., Lin, M., Grace, M., Pramanik, B., and Reinhold, V. N. (2007) Carbohydrate structural isomers analyzed by sequential mass spectrometry. Anal. Chem. 79, 3830-3842
35. Mizuochi, T., Hamako, J., and Titani, K. (1987) Structures of the sugar chains of mouse immunoglobulin G. Arch. Biochem. Biophys. 257, 387-394
36. Zhao, Y., Itoh, S., Wang, X., Isaji, T., Miyoshi, E., Kariya, Y., Miyazaki, K., Kawasaki, N., Taniguchi, N., and Gu, J. (2006) Deletion of core fucosylation on α3β1 integrin down-regulates its functions. J. Biol. Chem. 281, 38343-38350
37. Schachter, H. (1986) Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem. Cell Biol. 64, 163-181
38. Gu, J., Nishikawa, A., Tsuruoka, N., Ohno, M., Yamaguchi, N., Kangawa, K., and Taniguchi, N. (1993) Purification and characterization of UDP-N-acetylglucosamine: α-6-D-mannoside β1-6N- acetylglucosaminyltransferase (Nacetylglucosaminyltransferase V) from a human lung cancer cell line. J. Biochem. 113, 614-619
39. Reiss, K., Maretzky, T., Ludwig, A., Tousseyn, T., de Strooper, B., Hartmann, D., and Saftig, P. (2005) ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and β-catenin nuclear signalling. EMBO J. 24, 742-752
40. Liu, C., Li, Y., Semenov, M., Han, C., Baeg, G. H., Tan, Y., Zhang, Z., Lin, X., and He, X. (2002) Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847
41. Chen, C. Y., Jan, Y. H., Juan, Y. H., Yang, C. J., Huang, M. S., Yu, C. J., Yang, P. C., Hsiao, M., Hsu, T. L., and Wong, C. H. (2013) Fucosyltransferase 8 as a functional regulator of nonsmall cell lung cancer. Proc. Natl. Acad. Sci. U.S.A. 110, 630-635
42. Iijima, J., Zhao, Y., Isaji, T., Kameyama, A., Nakaya, S., Wang, X., Ihara, H., Cheng, X., Nakagawa, T., Miyoshi, E., Kondo, A., Narimatsu, H., Taniguchi, N., and Gu, J. (2006) Cell-cell interaction-dependent regulation of N-acetylglucosaminyltransferase III and the bisected N-glycans in GE11 epithelial cells. Involvement of E-cadherin-mediated cell adhesion. J. Biol. Chem. 281, 13038-13046
43. Nairn, A. V., York, W. S., Harris, K., Hall, E. M., Pierce, J. M., and Moremen, K. W. (2008) Regulation of glycan structures in animal tissues: transcript profiling of glycan-related genes. J. Biol. Chem. 283, 17298-17313
44. Naito, Y., Takematsu, H., Koyama, S., Miyake, S., Yamamoto, H., Fujinawa, R., Sugai, M., Okuno, Y., Tsujimoto, G., Yamaji, T., Hashimoto, Y., Itohara, S., Kawasaki, T., Suzuki, A., and Kozutsumi, Y. (2007) Germinal center marker GL7 probes activation-dependent repression ofN-glycolylneuraminic acid, a sialic acid species involved in the negative modulation of B-cell activation. Mol. Cell Biol. 27, 3008-3022
45. Funato, Y., Michiue, T., Asashima, M., and Miki, H. (2006) The thioredoxin- related redox-regulating protein nucleoredoxin inhibits Wnt-β- catenin signalling through dishevelled. Nat. Cell Biol. 8, 501-508
46. Grewal, P. K., McLaughlan, J. M., Moore, C. J., Browning, C. A., and Hewitt, J. E. (2005) Characterization of the LARGE family of putative glycosyltransferases associated with dystroglycanopathies. Glycobiology 15, 912-923
47. Chui, D., Oh-Eda, M., Liao, Y. F., Panneerselvam, K., Lal, A., Marek, K. W., Freeze, H. H., Moremen, K. W., Fukuda, M. N., and Marth, J. D. (1997) α-Mannosidase-II deficiency results in dyserythropoiesis and unveils an alternate pathway in oligosaccharide biosynthesis. Cell 90, 157-167
48. Takamatsu, S., Antonopoulos, A., Ohtsubo, K., Ditto, D., Chiba, Y., Le, D. T., Morris, H. R., Haslam, S. M., Dell, A., Marth, J. D., and Taniguchi, N. (2010) Physiological and glycomic characterization of N- acetylglucosaminyltransferase- IVa and -IVb double deficient mice. Glycobiology 20, 485-497