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Branched N-glycans and their implications for cell adhesion, signaling and clinical applications for cancer biomarkers and in therapeutics

  • Taniguchi, Naoyuki (Disease Glycomics Team, Systems Glycobiology Research Group, RIKEN Advanced Science Institute) ;
  • Korekane, Hiroaki (Disease Glycomics Team, Systems Glycobiology Research Group, RIKEN Advanced Science Institute)
  • Received : 2011.12.02
  • Published : 2011.12.31
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Abstract

Branched N-glycans are produced by a series of glycosyltransferases including N-acetylglucosaminyltransferases and fucosyltransferases and their corresponding genes. Glycans on specific glycoproteins, which are attached via the action of glycosyltransferases, play key roles in cell adhesion and signaling. Examples of this are adhesion molecules or signaling molecules such as integrin and E-cadherin, as well as membrane receptors such as the EGF and TGF-${\beta}$ receptors. These molecules also play pivotal roles in the underlying mechanism of a variety of disease such as cancer metastasis, diabetes, and chronic obstructive pulmonary disease (COPD). Alterations in the structures of branched N-glycans are also hall marks and are useful for cancer biomarkers and therapeutics against cancer. This mini-review describes some of our recent studies on a functional glycomics approach to the study of branched N-glycans produced by N-acetylglucosaminyltransferases III, IV, V and IX (Vb) (GnT-III, GnT-IV, V and IX (Vb)) and fucosyltransferase 8 (Fut8) and their pathophysiological significance, with emphasis on the importance of a systems glycobiology approach as a future perspective for glycobiology.

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References

  1. Apweiler, R., Hermjakob, H. and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biopys. Acta. 1473, 4-8. https://doi.org/10.1016/S0304-4165(99)00165-8
  2. Taniguchi, N., Ekuni, A., Ko, J. H., Miyoshi, E., Ikeda, Y., Ihara, Y., Nishikawa, A., Honke, K. and Takahashi, M. (2001) A glycomic approach to the identification and characterization of glycoprotein function in cells transfected with glycosyltransferase genes. Proteomics 1, 239-247. https://doi.org/10.1002/1615-9861(200102)1:2<239::AID-PROT239>3.0.CO;2-K
  3. Taniguchi, N., Takahashi, M., Miyoshi, E., Gu, J. and Matsumoto, A. (2004) Functional glycomics and evidence for gain- and loss-of-functions of target proteins for glycosyltransferases involved in N-glycan biosynthesis: their pivotal roles in growth and development, cancer metastasis and antibody therapy against cancer proceedings of the Japan Academy. Series B 80, 82-91.
  4. Taniguchi, N., Ihara, S., Saito, T., Miyoshi, E., Ikeda, Y. and Honke, K. (2001) Implication of GnT-V in cancer metastasis: a glycomic approach for identification of a target protein and its unique function as an angiogenic cofactor. Glycoconj. J. 18, 859-865. https://doi.org/10.1023/A:1022292223878
  5. Taniguchi, N., Miyoshi, E., Ko, J. H., Ikeda, Y. and Ihara, Y. (1999) Implication of N-acetylglucosaminyltransferases III and V in Cancer: Gene regulation and signaling mechanism. Biochim. Biophys. Acta (Review). 1473, 9-20. https://doi.org/10.1016/S0304-4165(99)00166-X
  6. Zhao, Y., Sato, Y., Isaji, T., Fukuda, T., Matsumoto, A., Miyoshi, E., Gu, J. and Taniguchi, N. (2008) Branched N-glycans regulate the biological functions of integrins and cadherins. FEBS J. 275, 1939-1948. https://doi.org/10.1111/j.1742-4658.2008.06346.x
  7. Zhao, Y. Y., Takahashi, M., Gu, J., Miyoshi, E., Matsumoto, A., Kitazume, S. and Taniguchi, N. (2008) Functional roles of N-glycans in cell signaling and cell adhesion in cancer. Cancer Sci. 99, 1304-1310. https://doi.org/10.1111/j.1349-7006.2008.00839.x
  8. Taniguchi, N. (2009) From the gamma-glutamyl cycle to the glycan cycle: a road with many turns and pleasant surprises. J. Biol. Chem. 284, 34469-34478. https://doi.org/10.1074/jbc.X109.023150
  9. Schachter, H. (1986) Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem. Cell Biol. 64, 163-181. https://doi.org/10.1139/o86-026
  10. Stanley, P., Schachter, H. and Taniguchi, N. (2009) N-Glycans; In Essentials of Glycobiology. 2nd ed: pp. 101-114 Cold Spring Harbor Laboratory Press, New York, USA.
  11. Narasimhan, S. (1982) Control of glycoprotein synthesis. UDP-GlcNAc: glycopeptide beta 4-N-acetylglucosaminyltransferase III, an enzyme in hen oviduct which adds GlcNAc in beta 1-4 linkage to the beta-linked mannose of the trimannosyl core of N-glycosyl oligosaccharides. J. Biol. Chem. 257, 10235-10242.
  12. Gleeson, P. A. and Schachter, H. (1983) Oligosaccharide branching of glycoproteins: biosynthetic mechanisms and possible biological functions. J. Biol. Chem. 258, 6162-6173.
  13. Taniguchi, N. and Ikeda, Y. (1998) Gamma-Glutamyl transpeptidase: catalytic mechanism and gene expression. Adv. Enzymol. Related Areas Mol. Biol. 72, 239-278.
  14. Yokosawa, N., Taniguchi, N., Tsukada, Y. and Makita, A. (1981) Physiochemical and immunochemical characterization of gamma-glutamyl transpeptidase from yolk sak tumor and ascitic hepatoma (AH-66) cells. Oncodev. Biol. Med. 2, 165-177.
  15. Yamashita, K., Hitoi, A., Taniguchi, N., Yokosawa, N., Tsukada, Y. and Kobata, A. (1983) Comparative study of the sugar chains of gamma-glutamyltranspeptidases purified from rat liver and rat AH-66 hepatoma cells. Cancer Res. 43, 5059-5063.
  16. Hase, S., Ibuki, T. and Ikenaka, T. (1984) Reexamination of the pyridylamination used for fluorescence labeling of oligosaccharides and its application to glycoproteins. J. Biochem. 95, 197-203. https://doi.org/10.1093/oxfordjournals.jbchem.a134585
  17. Nishikawa, A., Fujii, S., Sugiyama, T. and Taniguchi, N. (1988) A method for the determination of N-acetylglucosaminyltransferase III activity in rat tissues involving HPLC. Anal. Biochem. 170, 349-354. https://doi.org/10.1016/0003-2697(88)90641-0
  18. Taniguchi, N., Nishikawa, A., Fujii, S. and Gu, J. (1989) Glycosyltransferase assays using pyridylaminated acceptors: N-acetylglucosaminyltransferase III, IV, and V. Methods Enzymol. 179, 397-408. https://doi.org/10.1016/0076-6879(89)79139-4
  19. 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. https://doi.org/10.1016/0304-4165(90)90094-D
  20. Nishikawa, A., Ihara, Y., Hatakeyama, M., Kangawa, K. and Taniguchi, N. (1992) Purification, cDNA cloning, and expression of UDP-N-acetylglucosamine: alpha-D-mannoside beta-1, 4N-acetylglucosaminyltransferase III from rat kidney. J. Biol. Chem. 267, 18199-18204.
  21. Taniguchi, N., Mizoshi, E., Gu, J., Honke, K. and Matsumoto, A. (2006), Decoding sugar functions by identifying target glycoproteins. Curr. Opin. Struct. Biol. 6, 561-566.
  22. Yoshimura, M., Nishikawa, A., Ihara, Y., Taniguchi, S. and Taniguchi, N. (1995) Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc. Natl. Acad. Sci. U.S.A. 92, 8754-8758. https://doi.org/10.1073/pnas.92.19.8754
  23. 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. https://doi.org/10.1074/jbc.271.23.13811
  24. Pinho, S. S., Seruca, R., Gartner, F., Yamaguchi, Y., Gu, J., Taniguchi, N. and Reis, C. A. (2010) Modulation of E-cadherin function and dysfunction by N-glycosylation. Cell Mol. Life Sci. 68, 1011-1020.
  25. Iijima, J., Zhao, Y., Isaji, T., Kameyama, A., Nakaya, S., Wang, X., Ihara, H., Cheng, X., Nakagawa, T., Miyoshi, E. and Kondo, A. (2006) Cell-cell interaction-dependent regulation of N-acetylglucosaminyltransferase III and the bisected N-glycans in GEii epithelial cells. Involvement of E-cadherin-mediated cell adhesion. J. Biol. Chem. 281, 13038-13046. https://doi.org/10.1074/jbc.M601961200
  26. Isaji, T., Kariya, Y., Xu, Q., Fukuda, T., Taniguchi, N. and Gu, J. (2010) Functional roles of the bisecting GlcNAc in integrin-mediated cell adhesion. Methods Enzymol. 480, 445-459. https://doi.org/10.1016/S0076-6879(10)80019-9
  27. 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 alpha3beta1 integrin-mediated cell migration. J. Biol. Chem. 281, 32122-32130. https://doi.org/10.1074/jbc.M607274200
  28. Sato, Y., Isaji, T., Tajiri, M., Yoshida-Yamamoto, S., Yoshinaka, T., Somehara, T., Fukuda, T., Wada, Y. and Gu, J. (2001) An N-glycosylation site on the beta-propeller domain of the integrin alpha5 subunit plays key roles in both its function and site-specific modification by beta1,4-N-acetylglucosaminyltransferase III. J. Biol. Chem. 276, 11956-11962. https://doi.org/10.1074/jbc.M008551200
  29. Kariya, Y., Kawamura, C., Tabei, T. and Gu, J. (2010) Bisecting GlcNAc residues on laminin-332 down-regulate galectin-3-dependent keratinocyte motility. J. Biol. Chem. 286, 4310-4318.
  30. Sato, Y., Takahashi, M., Shibukawa, Y., Jain, S. K., Hamaoka, R., Miyagawa, J., Yaginuma, Y., Honke, K., Ishikawa, M. and Taniguchi, N. (2001) Overexpression of N-acetylglucosaminyltransferase III enhances the epidermal growth factor-induced phosphorylation of ERK in HeLaS3 cells by up-regulation of the internalization rate of the receptors. J. Biol. Chem. 276, 11956-11962. https://doi.org/10.1074/jbc.M008551200
  31. Takahashi, M., Tsuda, T., Ikeda, Y., Honke, K. and Taniguchi, N. (2004) Role of N-glycans in growth factor signaling. Glycoconj. J. 20, 207-212.
  32. 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. https://doi.org/10.1016/j.carres.2009.04.031
  33. Ihara, Y., Sakamoto, Y., Mihara, M., Shimizu, K. and Taniguchi, N. (1997) Overexpression of N-acetylglucosaminyltransferase III disrupts the tyrosine phosphorylation of Trk with resultant signaling dysfunction in PC12 cells treated with nerve growth factor. J. Biol. Chem. 272, 9629-9634. https://doi.org/10.1074/jbc.272.15.9629
  34. Xu, Q., Akama, R., Isaji, T., Lu, Y., Hashimoto, H., Kariya, Y., Fukuda, T., Du, Y. and Gu, J. (2011) Wnt/beta-catenin signaling down-regulates N-acetylglucosaminyltransferase III expression: the implications of two mutually exclusive pathways for regulation. J. Biol. Chem. 286, 4310-4318. https://doi.org/10.1074/jbc.M110.182576
  35. Shibukawa, Y., Takahashi, M., Laffont, I., Honke, K. and Taniguchi, N. (2003) Down-regulation of hydrogen peroxide- induced PKC delta activation in N-acetylglucosaminyltransferase III-transfected HeLaS3 cells. J. Biol. Chem. 278, 3197-3203. https://doi.org/10.1074/jbc.M207870200
  36. Li, W., Takahashi, M., Shibukawa, Y., Yokoe, S., Gu, J., Miyoshi, E., Honke, K., Ikeda, Y. and Taniguchi, N. (2007) Introduction of bisecting GlcNAc in N-glycans of adenylyl cyclase III enhances its activity. Glycobiology 17, 655-662. https://doi.org/10.1093/glycob/cwm022
  37. Yoshimura, M., Ihara, Y., Ohnishi, A., Ijuhin, N., Nishiura, T., Kanakura, Y., Matsuzawa, Y. and Taniguchi, N. (1996) Bisecting N-acetylglucosamine on K562 cells suppresses natural killer cytotoxicity and promotes spleen colonization. Cancer Res. 56, 412-418.
  38. Gu, J., Zhao, Y., Isaji, T., Shibukawa, Y., Ihara, H., Takahashi, M., Ikeda, Y., Miyoshi, E., Honke, K. and Taniguchi, N. (2004) beta1,4-N-Acetylglucosaminyltransferase III down-regulates neurite outgrowth induced by costimulation of epidermal growth factor and integrins through the Ras/ERK signaling pathway in PC12 cells. Glycobiology 14, 177-186.
  39. Guo, H. B., Jiang, A. L., Ju, T. Y. and Chen, H. L. (2000) Opposing changes in N-acetylglucosaminyltransferase-V and -III during the cell cycle and all-trans retinoic acid treatment of hepatocarcinoma cell line. Biochim. Biophys. Acta 1495, 297-307. https://doi.org/10.1016/S0167-4889(99)00157-3
  40. Koma, M., Miyagawa, S., Honke, K., Ikeda, Y., Koyota, S., Miyoshi, S., Matsuda, H., Tsuji, S., Shirakura, R. and Taniguchi, N. (2000) Reduction of the major xenoantigen on glycosphingolipids of swine endothelial cells by various glycosyltransferases. Glycobiology 10, 745-751. https://doi.org/10.1093/glycob/10.7.745
  41. Koyota, S., Ikeda, Y., Miyagawa, S., Ihara, H., Koma, M., Honke, K., Shirakura, R. and Taniguchi, N. (2001) Down-regulation of the alpha-Gal epitope expression in N-glycans of swine endothelial cells by transfection with the N-acetylglucosaminyltransferase III gene. Modulation of the biosynthesis of terminal structures by a bisecting GlcNAc. J. Biol. Chem. 276, 32867-32874. https://doi.org/10.1074/jbc.M102371200
  42. Komoda, H., Miyagawa, S., Omori, T., Takahagi, Y., Murakami, H., Shigehisa, T., Ito, T., Matsuda, H. and Shirakura, R. (2005) Survival of adult islet grafts from transgenic pigs with N-acetylglucosaminyltransferase-III (GnT-III) in cynomolgus monkeys. Xenotransplantation (3), 209-216.
  43. Oguri, S., Minowa, M. T., Ihara, Y., Taniguchi, N., Ikenaga, H. and Takeuchi, M. (1997) Purification and characterization of UDP-N-acetylglucosamine: alpha 1,3-D-mannoside beta 1,4- N-acetylglucosaminyltransferase (N-acetylglucosaminyltransferase-IV) from bovine small intestine. J. Biol. Chem. 272, 22721-22727. https://doi.org/10.1074/jbc.272.36.22721
  44. Minowa, M. T., Oguri, S., Yoshida, A., Hara, T., Iwamatsu, A., Ikenaga, H. and Takeuchi, M. (1998) cDNA cloning and expression of bovine UDP-N-acetylglucosamine: alpha1,3-D-mannoside beta1,4-N-acetylglucosaminyltransferase IV. J. Biol. Chem. 273, 11556-11562. https://doi.org/10.1074/jbc.273.19.11556
  45. Yamashita, K., Totani, K., Iwaki, Y., Takamisawa, I., Tateishi, N., Higashi, T., Sakamoto, Y. and Kobata, A.(1989) Comparative study of the sugar chains of gamma-glutamyltranspeptidases purified from human hepatocellular carcinoma and from human liver. J. Biochem. 1105, 728-735.
  46. Endo, T., Nishimura, R., Kawano, T., Mochizuki, M. and Kobata, A. (1987) Structural differences found in the asparagine-linked sugar chains of human chorionic gonadotropins purified from the urine of patients with invasive mole and with choriocarcinoma. Cancer Res. 47, 5242-5245.
  47. Koenderman, A. H., Koppen, P. L., Koeleman, C. A. and van den Eijnden, D. H. (1989) N-acetylglucosaminyltransferase III, IV and V activities in Novikoff ascites tumour cells, mouse lymphoma cells and hen oviduct. Application of a sensitive and specific assay by use of high-performance liquid chromatography. Eur. J. Biochem. 181, 651-655. https://doi.org/10.1111/j.1432-1033.1989.tb14772.x
  48. Nakao, H., Nishikawa, A., Karasuno, T., Nishiura, T., Iida, M., Kanayama, Y., Yonezawa, T., Tarui, S. and Taniguchi, N. (1990) Modulation of N-acetylglucosaminyltransferase III, IV and V activities and alteration of the surface oligosaccharide structure of a myeloma cell line by interleukin 6. Biochem. Biophys. Res. Commun. 172, 1260-1266. https://doi.org/10.1016/0006-291X(90)91585-G
  49. Ide, Y., Gu, J., Tanemura, M., Nishida, T., Ito, T., Yamamoto, H., Kozutsumi, Y. and Taniguchi, N (2006) Aberrant expression of N-acetylglucosaminyltransferase-IVa and IVb (GnT-IVa and b) in pancreatic cancer. Biochem. Biophys. Res. Commun. 341, 478-482. https://doi.org/10.1016/j.bbrc.2005.12.208
  50. Ohtsubo, K. (2010) Targeted genetic inactivation N-acetylglucosaminyltransferase-IVa impairs insulin secretion from pancreatic beta cells and evokes type 2 diabetes. Methods Enzymol. 479, 205-222. https://doi.org/10.1016/S0076-6879(10)79012-1
  51. Ohtsubo, K., Chen, M. Z., Olefsky, J. M. and Marth, J. D. (2011) Pathway to diabetes through attenuation of pancreatic beta cell glycosylation and glucose transport. Nat. Med. 17, 1067-1075. https://doi.org/10.1038/nm.2414
  52. Takamatsu, S., Antonopoulos, A., Ohtubo, 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 4, 485-497.
  53. Shoreibah, M., Perng, G. S., Adler, B., Weinstein, J., Basu, R., Cupples, R., Wen, D., Browne, J. K., Buckhaults, P., Fregien, N. and Pierce, M. (1993) Isolation, characterization, and expression of a cDNA encoding N-acetylglucosaminyltransferase V. J. Biol. Chem. 268, 15381-15385.
  54. Gu, J., Nishikawa, A., Tsuruoka, N., Ohno, M., Yamaguchi, N., Kangawa, K. and Taniguchi, N. (1993) Purification and characterization of UDP-N-acetylglucosamine: alpha-6-Dmannoside beta 1-6N-acetylglucosaminyltransferase (N-acetylglucosaminyltransferase V) from a human lung cancer cell line. J. Biochem. 113, 614-619. https://doi.org/10.1093/oxfordjournals.jbchem.a124091
  55. Granovsky, M., Fata, J., Pawling, J., Muller, W. J., Khokha, R. and Dennis, J. W. (2000) Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat. Med. 6, 306-312. https://doi.org/10.1038/73163
  56. Partridge, E. A., Le Roy, C., Di Guglielmo, G. M., Pawling, J., Cheung, P., Granovsky, M., Nabi, I. R., Wrana, J. L. and Dennis, J. W. (2004) Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science 306, 120-124. https://doi.org/10.1126/science.1102109
  57. Lau, K. S., Partridge, E. A., Grigorian, A., Silvescu, C. I., Reinhold, V. N., Demetriou, M. and Dennis, J. W. (2007) Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129, 123-134. https://doi.org/10.1016/j.cell.2007.01.049
  58. Taniguchi, N., Ihara, S., Saito, T., Miyoshi, E., Ikeda, Y. and Honke, K. (2001) Implication of GnT-V in cancer metastasis: a glycomic approach for identification of a target protein and its unique function as an angiogenic cofactor. Glycoconj. J. 18, 859-865. https://doi.org/10.1023/A:1022292223878
  59. Kang, R., Saito, H., Ihara, Y., Miyoshi, E., Koyama, N., Sheng, Y. and Taniguchi, N. (1996) Transcriptional regulation of the N-acetylglucosaminyltransferase V gene in human bile duct carcinoma cells (HuCC-T1) is mediated by Ets-1. J. Biol. Chem. 271, 26706-26712. Erratum in: J. Biol. Chem. (1999) 274, 554. https://doi.org/10.1074/jbc.271.43.26706
  60. Ko, J. H., Miyoshi, E., Noda, K., Ekuni, A., Kang, R., Ikeda, Y. and Taniguchi, N. (1999) Regulation of the GnT-V promoter by transcription factor Ets-1 in various cancer cell lines. J. Biol. Chem. 274, 22941-22948. https://doi.org/10.1074/jbc.274.33.22941
  61. Miyoshi, E., Nishikawa, A., Ihara, Y., Saito, H., Uozumi, N., Hayashi, N., Fusamoto, H., Kamada, T. and Taniguchi, N. (1995) Transforming growth factor beta up-regulates expression of the N-acetylglucosaminyltransferase V gene in mouse melanoma cells. J. Biol. Chem. 270, 6216-6220. https://doi.org/10.1074/jbc.270.11.6216
  62. Guo, HB., Lee, I., Kamar, M. and Pierce, M. (2003) N-acetylglucosaminyltransferase V expression levels regulate cadherin-associated homotypic cell-cell adhesion and intracellular signaling pathways. J. Biol. Chem. 278, 52412-52424. https://doi.org/10.1074/jbc.M308837200
  63. Sato, T. and Furukawa, K. (1995) Sequential action of Ets-1 and Sp1 in the activation of the human beta-1,4-galactosyltransferase V gene involved in abnormal glycosylation characteristic of cancer cells. J. Biol. Chem. 270, 6216-6220. https://doi.org/10.1074/jbc.270.11.6216
  64. Zhang, W., Revers, L., Pierce, M. and Schachter, H. (2000) Regulation of expression of the human beta-1, 2-N-acetylglucosaminyltransferase II gene (MGAT2) by Ets transcription factors. Biochem. J. 347(Pt 2), 511-518. https://doi.org/10.1042/0264-6021:3470511
  65. Ihara, S., Miyoshi, E., Ko, J. H., Murata, K., Nakahara, S., Honke, K., Dickson, R. B., Lin, C. Y. and Taniguchi, N. (2002) Prometastatic effect of N-acetylglucosaminyltransferase V is due to modification and stabilization of active matriptase by adding beta 1-6 GlcNAc branching. J. Biol. Chem. 277, 16960-16967. https://doi.org/10.1074/jbc.M200673200
  66. Ihara, S., Miyoshi, E., Nakahara, S., Sakiyama, H., Ihara, H., Akinaga, A., Honke, K., Dickson, RB, Lin, C. Y. and Taniguchi, N. (2004) Addition of beta1-6 GlcNAc branching to the oligosaccharide attached to Asn 772 in the serine protease domain of matriptase plays a pivotal role in its stability and resistance against trypsin. Glycobiology 14, 139-146.
  67. Kataoka, H., Miyata, S., Uchinokura, S. and Itoh, H. (2003) Roles of hepatocyte growth factor (HGF) activator and HGF activator inhibitor in the pericellular activation of HGF/scatter factor. Cancer Metastasis Rev. 22, 223-236. https://doi.org/10.1023/A:1023051500010
  68. Santin, A. D., Cane', S., Bellone, S., Bignotti, E., Palmieri, M., De Las Casas, L. E., Anfossi, S., Roman, J. J., O'Brien, T. and Pecorelli, S. (2003) The novel serine protease tumor-associated differentially expressed gene-15 (matriptase/MT-SP1) is highly overexpressed in cervical carcinoma. Cancer 98, 1898-1904. https://doi.org/10.1002/cncr.11753
  69. Saito, T., Miyoshi, E., Sasai, K., Nakano, N., Eguchi, H., Honke, K. and Taniguchi, N. (2002) A secreted type of beta 1, 6-N-acetylglucosaminyltransferase V (GnT-V) induces tumor angiogenesis without mediation of glycosylation: a novel function of GnT-V distinct from the original glycosyltransferase activity. J. Biol. Chem. 277, 17002-17008. https://doi.org/10.1074/jbc.M200521200
  70. Nakahara, S., Saito, T., Kondo, N., Moriwaki, K., Noda, K., Ihara, S., Takahashi, M., Ide, Y., Gu, J., Inohara, H., Katayama, T., Tohyama, M., Kubo, T., Taniguchi, N. and Miyoshi, E. (2006) A secreted type of beta1, 6 N-acetylglucosaminyltransferase V (GnT-V), a novel angiogenesis inducer, is regulated by gamma-secretase. FASEB J. 14, 2451-2459. Erratum in: FASEB J. 21, 630.
  71. Terao, M., Ishikawa, A., Nakahara, S., Kimura, A., Kato, A., Moriwaki, K., Kamada, Y., Murota, H., Taniguchi, N., Katayama, I. and Miyoshi, E. (2011) Enhanced epithelial-mesenchymal transition-like phenotype in N-acetylglucosaminyltransferase V transgenic mouse skin promotes wound healing. J. Biol. Chem. 286, 28303-28311. https://doi.org/10.1074/jbc.M111.220376
  72. Kim, Y. S., Hwang, S. Y., Kang, H. Y., Sohn, H., Oh, S., Kim, J. Y., Yoo, J. S., Kim, Y. H., Kim, C. H., Jeon, J. H., Lee, J. M., Kang, H. A., Miyoshi, E., Taniguchi, N., Yoo, H. S. and Ko, J. H. (2008) Functional proteomics study reveals that N-Acetylglucosaminyltransferase V reinforces the invasive/metastatic potential of colon cancer through aberrant glycosylation on tissue inhibitor of metalloproteinase-1. Mol. Cell Proteomics. 7, 1-14. https://doi.org/10.1074/mcp.M700084-MCP200
  73. Inamori, K., Endo, T., Ide, Y., Fujii, S., Gu, J., Honke, K. and Taniguchi, N. (2003) Molecular cloning and characterization of human GnT-IX, a novel beta1, 6-N-acetylglucosaminyltransferase that is specifically expressed in the brain. J. Biol. Chem. 278, 43102-43109. https://doi.org/10.1074/jbc.M308255200
  74. Kaneko, M., Alvarez-Manilla, G., Kamar, M., Lee, I., Lee, J. K., Troupe, K., Zhang, W., Osawa, M. and Pierce, M. (2003) A novel beta(1,6)-N-acetylglucosaminyltransferase V (GnTVB). FEBS Lett. 554, 515-519. https://doi.org/10.1016/S0014-5793(03)01234-1
  75. Inamori, K., Endo, T., Gu, J., Matsuo, I., Ito, Y., Fujii, S., Iwasaki, H., Narimatsu, H., Miyoshi, E., Honke, K. and Taniguchi, N. (2004) N-Acetylglucosaminyltransferase IX acts on the GlcNAc beta 1, 2-Man alpha 1-Ser/Thr moiety, forming a 2, 6-branched structure in brain O-mannosyl glycan. J. Biol. Chem. 279, 2337-2340. https://doi.org/10.1074/jbc.C300480200
  76. Inamori, K., Gu, J., Ohira, M., Kawasaki, A., Nakamura, Y., Nakagawa, T., Kondo, A., Miyoshi, E., Nakagawara, A. and Taniguchi, N. (2006) High expression of N-acetylglucosaminyltransferase V in favorable neuroblastomas: Involvement of its effect on apoptosis. FEBS Lett. 580, 627-632. https://doi.org/10.1016/j.febslet.2005.12.089
  77. Inamori, K., Mita, S., Gu, J., Mizuno-Horikawa, Y., Miyoshi, E., Dennis, J. W. and Taniguchi, N. (2006) Demonstration of the expression and the enzymatic activity of N-acetylglucosaminyltransferase IX in the mouse brain. Biochim. Biophys. Acta 60, 678-684.
  78. Kizuka, Y., Kitazume, S., Yoshida, M. and Taniguchi, N. (2011) Brain-specific expression of N-acetylglucosaminyltransferase IX (GnT-IX) is regulated by epigenetic histone modifications. J. Biol. Chem. 286, 31875-31884. https://doi.org/10.1074/jbc.M111.251173
  79. Chiba, A., Matsumura, K., Yamada, H., Inazu, T., Shimizu, T., Kusunoki, S., Kanazawa, I., Kobata, A. and Endo, T. (1997) Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve alpha-dystroglycan. The role of a novel Omannosyl- type oligosaccharide in the binding of alpha-dystroglycan with laminin. J. Biol. Chem. 272, 2156-2162. https://doi.org/10.1074/jbc.272.4.2156
  80. Matsumura, K. and Campbell, K. P. (1994) Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 1, 2-15.
  81. Toda, T., Chiyonobu, T., Xiong, H., Tachikawa, M., Kobayashi, K., Manya, H., Takeda, S., Taniguchi, M., Kurahashi, H. and Endo, T. (2005) Fukutin and alpha-dystroglycanopathies. Acta Myol. 24, 60-63.
  82. Abbott, K. L., Matthews, R. T. and Pierce, M. (2008) Receptor tyrosine phosphatase beta (RPTPbeta) activity and signaling are attenuated by glycosylation and subsequent cell surface galectin-1 binding. J. Biol. Chem. 283, 33026-33035. https://doi.org/10.1074/jbc.M803646200
  83. Oriol, R., Mollicone, R., Cailleau, A., Balanzino, L. and Breton, C. (1999) Divergent evolution of fucosyltransferase genes from vertebrates, invertebrates, and bacteria. Glycobiology 9, 323-334. https://doi.org/10.1093/glycob/9.4.323
  84. Voynow, J. A., Kaiser, R. S., Scanlin, T. F. and Glick, M. C. (1991) Purification and characterization of GDP-L-fucose-Nacetyl beta-D-glucosaminide alpha 1-6fucosyltransferase from cultured human skin fibroblasts. Requirement of a specific biantennary oligosaccharide as substrate. J. Biol. Chem. 266, 21572-21577.
  85. 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-beta-D-glucosaminide alpha1-6fucosyltransferase. J. Biol. Chem. 271, 27810-27817. https://doi.org/10.1074/jbc.271.44.27810
  86. Yanagidani, S., Uozumi, N., Ihara, Y., Miyoshi, E., Yamaguchi, N. and Taniguchi, N. (1997) Purification and cDNA cloning of GDP-L-Fuc:N-acetyl-beta-D-glucosaminide:alpha1-6 fucosyltransferase (alpha1-6 FucT) from human gastric cancer MKN45 cells. J. Biochem. 121, 626-632. https://doi.org/10.1093/oxfordjournals.jbchem.a021631
  87. 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-beta1 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. https://doi.org/10.1073/pnas.0507375102
  88. Yamada, M., Ishii, T., Ikeda, S., Naka-Mieno, M., Tanaka, N., Arai, T., Kumasaka, T., Gemma, A., Kida, K., Muramatsu, M. and Sawabe, M. (2011) Association of fucosyltransferase 8 (FUT8) polymorphism Thr267Lys with pulmonary emphysema. J. Hum. Gen. (in press).
  89. Fukuda, T., Hashimoto, H., Okayasu, N., Kameyama, A., Onogi, H., Nakagawasai, O., Nakazawa, T., Kurosawa, T., Hao, Y., Isaji, T., Tadano, T., Narimatsu, H., Taniguchi, N. and Gu, J. (2011) Alpha1, 6-fucosyltransferase-deficient mice exhibit multiple behavioral abnormalities associated with a schizophrenia-like phenotype: importance of the balance between the dopamine and serotonin systems. J. Biol. Chem. 286, 18434-18443. https://doi.org/10.1074/jbc.M110.172536
  90. Aoyagi, Y., Suzuki, Y., Isemura, M., Nomoto, M., Sekine, C., Igarashi, K. and Ichida, F. (1988) The fucosylation index of alpha- fetoprotein and its usefulness in the early diagnosis of hepatocellular carcinoma. Cancer 61, 769-774. https://doi.org/10.1002/1097-0142(19880215)61:4<769::AID-CNCR2820610422>3.0.CO;2-M
  91. Taketa, K., Endo, Y., Sekiya, C., Tanikawa, K., Koji, T., Taga, H., Satomura, S., Matsuura, S., Kawai, T. and Hirai, H. (1993) A collaborative study for the evaluation of lectin-reactive alpha- fetoproteins in early detection of hepatocellular carcinoma. Cancer Res. 53, 5419-5423.
  92. Nakagawa, T., Miyoshi, E., Yakushijin, T., Hiramatsu, N., Igura, T., Hayashi, N., Taniguchi, N. and Kondo, A. (2008) Glycomic analysis of alpha-fetoprotein L3 in hepatoma cell lines and hepatocellular carcinoma patients. J. Proteome Res. 6, 2222-2233.
  93. Okuyama, N., Ide, Y., Nakano, M., Nakagawa, T., Yamanaka, K., Moriwaki, K., Murata, K., Ohigashi, H., Yokoyama, S., Eguchi, H., Ishikawa, O., Ito, T., Kato, M., Kasahara, A., Kawano, S., Gu, J., Taniguchi, N. and Miyoshi, E. (2006) Fucosylated haptoglobin is a novel marker for pancreatic cancer: a detailed analysis of the oligosaccharide structure and a possible mechanism for fucosylation. Int. J. Cancer 118, 2803-2808. https://doi.org/10.1002/ijc.21728
  94. Takeda, Y., Shinzaki, S., Okudo, K., Moriwaki, K., Murata, K. and Miyoshi, E. (2011) Fucosylated haptoglobin is a novel type of cancer biomarker linked to the prognosis after an operation in colorectal cancer. Cancer (in press).
  95. Nakagawa, T., Uozumi, N., Nakano, M., Mizuno-Horikawa, Y., Okuyama, N., Taguchi, T., Gu, J., Kondo, A., Taniguchi, N. and Miyoshi, E. (2006) Fucosylation of N-glycans regulates the secretion of hepatic glycoproteins into bile ducts. J. Biol. Chem. 281, 29797-29806. https://doi.org/10.1074/jbc.M605697200
  96. Shields, R. L., Lai, J., Keck, R., O'Connell, L. Y., Hong, K., Meng, Y. G., Weikert, S. H. and Presta, L. G. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J. Biol. Chem. 277, 26733-26740. https://doi.org/10.1074/jbc.M202069200
  97. 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. https://doi.org/10.1074/jbc.M210665200
  98. Ferrara, C., Grau, S., Jäger, C., Sondermann, P., Brünker, P., Waldhauer, I., Hennig, M., Ruf, A., Rufer, A. C., Stihle, M., Umaña, P. and Benz, J. (2011) Unique carbohydrate-carbohy-drate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc. Natl. Acad. Sci. U.S.A. 108, 12669-12674. https://doi.org/10.1073/pnas.1108455108
  99. Mizushima, T., Yagi, H., Takemoto, E., Shibata-Koyama, M., Isoda, Y., Iida, S., Masuda, K., Satoh, M. and Kato, K. (2011) Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans. Genes Cells 11, 1071-1080.
  100. Taniguchi, N. (2006) From glycobiology to systems glycobiology: International network with Japanese scientists through consortia. IUBMB Life 58, 1-4. https://doi.org/10.1080/15216540500484368

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