Skip to main content

Advertisement

Log in

Neural functions of bisecting GlcNAc

  • Mini-Review
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Bisecting GlcNAc, a branch structure in N-glycan, has unique functions and is involved in several diseases including Alzheimer’s disease (AD). In this review, we provide an overview of the biosynthesis of bisecting GlcNAc and its physiological and pathological functions, particularly in the nervous system where bisecting GlcNAc is most highly expressed. The biosynthetic enzyme of bisecting GlcNAc is N-acetylglucosaminyltransferase-III (GnT-III). Overexpression, knockdown, and knockout of GnT-III have so far revealed various functions of bisecting GlcNAc, which are mediated by regulating the functions of key carrier proteins. GnT-III-deficient AD model mice showed reduced amyloid-β (Aβ) accumulation in the brain by suppressing the function of a key Aβ-generating enzyme, β-site APP-cleaving enzyme-1 (BACE1), and greatly improved AD pathology. Altered BACE1 subcellular localization in GnT-III-deficient cells, from early endosomes to lysosomes, suggests that bisecting GlcNAc serves as a trafficking tag for the movement of modified proteins to an endosomal compartment. For therapeutic application, we have employed high-throughput screening to search for GnT-III inhibitors. These findings highlight the importance of bisecting GlcNAc modification in the nervous system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Varki, A.: Biological roles of glycans. Glycobiology. 27(1), 3–49 (2017). https://doi.org/10.1093/glycob/cww086

    Article  CAS  PubMed  Google Scholar 

  2. Moremen, K.W., Tiemeyer, M., Nairn, A.V.: Vertebrate protein glycosylation: diversity, synthesis and function. Nat. Rev. Mol. Cell Biol. 13(7), 448–462 (2012). https://doi.org/10.1038/nrm3383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ohtsubo, K., Marth, J.D.: Glycosylation in cellular mechanisms of health and disease. Cell. 126(5), 855–867 (2006). https://doi.org/10.1016/j.cell.2006.08.019

    Article  CAS  PubMed  Google Scholar 

  4. Takahashi, M., Kizuka, Y., Ohtsubo, K., Gu, J., Taniguchi, N.: Disease-associated glycans on cell surface proteins. Mol. Asp. Med. 51, 56–70 (2016). https://doi.org/10.1016/j.mam.2016.04.008

    Article  CAS  Google Scholar 

  5. Kizuka, Y., Taniguchi, N.: Enzymes for N-glycan branching and their genetic and nongenetic regulation in cancer. Biomolecules. 6(2), (2016). https://doi.org/10.3390/biom6020025

    Article  CAS  PubMed Central  Google Scholar 

  6. Takahashi, M., Kuroki, Y., Ohtsubo, K., Taniguchi, N.: Core fucose and bisecting GlcNAc, the direct modifiers of the N-glycan core: their functions and target proteins. Carbohydr. Res. 344(12), 1387–1390 (2009). https://doi.org/10.1016/j.carres.2009.04.031

    Article  CAS  PubMed  Google Scholar 

  7. Nishikawa, A., Ihara, Y., Hatakeyama, M., Kangawa, K., Taniguchi, N.: Purification, cDNA cloning, and expression of UDP-N-acetylglucosamine: beta-D-mannoside beta-1,4N-acetylglucosaminyltransferase III from rat kidney. J. Biol. Chem. 267(25), 18199–18204 (1992)

    CAS  PubMed  Google Scholar 

  8. Taniguchi, N., Kizuka, Y.: Glycans and cancer: role of N-glycans in cancer biomarker, progression and metastasis, and therapeutics. Adv. Cancer Res. 126, 11–51 (2015). https://doi.org/10.1016/bs.acr.2014.11.001

    Article  PubMed  Google Scholar 

  9. Taniguchi, N., Miyoshi, E., Gu, J., Honke, K., Matsumoto, A.: Decoding sugar functions by identifying target glycoproteins. Curr. Opin. Struct. Biol. 16(5), 561–566 (2006). https://doi.org/10.1016/j.sbi.2006.08.011

    Article  CAS  PubMed  Google Scholar 

  10. Taniguchi, N.: From the gamma-glutamyl cycle to the glycan cycle: a road with many turns and pleasant surprises. J. Biol. Chem. 284(50), 34469–34478 (2009). https://doi.org/10.1074/jbc.X109.023150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kizuka, Y., Kitazume, S., Fujinawa, R., Saito, T., Iwata, N., Saido, T.C., Nakano, M., Yamaguchi, Y., Hashimoto, Y., Staufenbiel, M., Hatsuta, H., Murayama, S., Manya, H., Endo, T., Taniguchi, N.: An aberrant sugar modification of BACE1 blocks its lysosomal targeting in Alzheimer's disease. EMBO Mol. Med. 7(2), 175–189 (2015). https://doi.org/10.15252/emmm.201404438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ohtsubo, K., Chen, M.Z., Olefsky, J.M., Marth, J.D.: Pathway to diabetes through attenuation of pancreatic beta cell glycosylation and glucose transport. Nat. Med. 17(9), 1067–1075 (2011). https://doi.org/10.1038/nm.2414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Granovsky, M., Fata, J., Pawling, J., Muller, W.J., Khokha, R., Dennis, J.W.: Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat. Med. 6(3), 306–312 (2000). https://doi.org/10.1038/73163

    Article  CAS  PubMed  Google Scholar 

  14. Ikeda, Y., Ihara, H., Tsukamoto, H., Gu, J., Taniguchi, N.: Mannosyl (Beta-1,4-)-glycoprotein Beta-1,4-N-Acetylglucosaminyltransferase (MGAT3); β1,4-N-Acetylglucosaminyltransferase III (GnT-III, GlcNAcT-III). In: Taniguchi, N., Honke, K., Fukuda, M., Narimatsu, H., Yamaguchi, Y., Angata, T. (eds.) Handbook of Glycosyltransferases and Related Genes, pp. 209–222. Springer Japan, Tokyo (2014)

    Chapter  Google Scholar 

  15. Miyoshi, E., Uozumi, N., Noda, K., Hayashi, N., Hori, M., Taniguchi, N.: Expression of alpha1-6 fucosyltransferase in rat tissues and human cancer cell lines. Int. J. Cancer. 72(6), 1117–1121 (1997)

    Article  CAS  PubMed  Google Scholar 

  16. Schachter, H.: Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem. Cell Biol. 64(3), 163–181 (1986)

    Article  CAS  PubMed  Google Scholar 

  17. Stanley, P., Schachter, H., Taniguchi, N.: N-Glycans. In: Varki, A., Cummings, R.D., Esko, J.D., Freeze, H.H., Stanley, P., Bertozzi, C.R., Hart, G.W., Etzler, M.E. (eds). Essentials of Glycobiology. Cold Spring Harbor (NY) (2009)

  18. Gu, J., Nishikawa, A., Tsuruoka, N., Ohno, M., Yamaguchi, N., Kangawa, K., Taniguchi, N.: Purification and characterization of UDP-N-acetylglucosamine: alpha-6-D-mannoside beta 1-6N-acetylglucosaminyltransferase (N-acetylglucosaminyltransferase V) from a human lung cancer cell line. J. Biochem. 113(5), 614–619 (1993)

    Article  CAS  PubMed  Google Scholar 

  19. Re, S., Miyashita, N., Yamaguchi, Y., Sugita, Y.: Structural diversity and changes in conformational equilibria of biantennary complex-type N-glycans in water revealed by replica-exchange molecular dynamics simulation. Biophys. J. 101(10), L44–L46 (2011). https://doi.org/10.1016/j.bpj.2011.10.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nagae, M., Kanagawa, M., Morita-Matsumoto, K., Hanashima, S., Kizuka, Y., Taniguchi, N., Yamaguchi, Y.: Atomic visualization of a flipped-back conformation of bisected glycans bound to specific lectins. Sci. Rep. 6, 22973 (2016). https://doi.org/10.1038/srep22973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fujii, S., Nishiura, T., Nishikawa, A., Miura, R., Taniguchi, N.: Structural heterogeneity of sugar chains in immunoglobulin G. Conformation of immunoglobulin G molecule and substrate specificities of glycosyltransferases. J. Biol. Chem. 265(11), 6009–6018 (1990)

    CAS  PubMed  Google Scholar 

  22. Taniguchi, N., Yoshimura, M., Miyoshi, E., Ihara, Y., Nishikawa, A., Fujii, S.: 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(7), 691–694 (1996)

    Article  CAS  PubMed  Google Scholar 

  23. Yoshimura, M., Nishikawa, A., Ihara, Y., Taniguchi, S., Taniguchi, N.: Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc. Natl. Acad. Sci. U. S. A. 92(19), 8754–8758 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Yoshimura, M., Ihara, Y., Matsuzawa, Y., Taniguchi, N.: Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J. Biol. Chem. 271(23), 13811–13815 (1996)

    Article  CAS  PubMed  Google Scholar 

  25. Priatel, J.J., Sarkar, M., Schachter, H., Marth, J.D.: Isolation, characterization and inactivation of the mouse Mgat3 gene: the bisecting N-acetylglucosamine in asparagine-linked oligosaccharides appears dispensable for viability and reproduction. Glycobiology. 7(1), 45–56 (1997)

    Article  CAS  PubMed  Google Scholar 

  26. Song, Y., Aglipay, J.A., Bernstein, J.D., Goswami, S., Stanley, P.: The bisecting GlcNAc on N-glycans inhibits growth factor signaling and retards mammary tumor progression. Cancer Res. 70(8), 3361–3371 (2010). https://doi.org/10.1158/0008-5472.CAN-09-2719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bhattacharyya, R., Bhaumik, M., Raju, T.S., Stanley, P.: Truncated, inactive N-acetylglucosaminyltransferase III (GlcNAc-TIII) induces neurological and other traits absent in mice that lack GlcNAc-TIII. J. Biol. Chem. 277(29), 26300–26309 (2002). https://doi.org/10.1074/jbc.M202276200

    Article  CAS  PubMed  Google Scholar 

  28. Lu, J., Isaji, T., Im, S., Fukuda, T., Kameyama, A., Gu, J.: Expression of N-acetylglucosaminyltransferase III suppresses alpha2,3 sialylation and its distinctive functions in cell migration are attributed to alpha2,6 sialylation levels. J. Biol. Chem. (2016). https://doi.org/10.1074/jbc.M115.712836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Koyota, S., Ikeda, Y., Miyagawa, S., Ihara, H., Koma, M., Honke, K., Shirakura, R., Taniguchi, N.: 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(35), 32867–32874 (2001). https://doi.org/10.1074/jbc.M102371200

    Article  CAS  PubMed  Google Scholar 

  30. Akasaka-Manya, K., Manya, H., Sakurai, Y., Wojczyk, B.S., Kozutsumi, Y., Saito, Y., Taniguchi, N., Murayama, S., Spitalnik, S.L., Endo, T.: Protective effect of N-glycan bisecting GlcNAc residues on beta-amyloid production in Alzheimer’s disease. Glycobiology. 20(1), 99–106 (2010). https://doi.org/10.1093/glycob/cwp152

    Article  CAS  PubMed  Google Scholar 

  31. Kizuka, Y., Nakano, M., Miura, Y., Taniguchi, N.: Epigenetic regulation of neural N-glycomics. Proteomics. 16(22), 2854–2863 (2016). https://doi.org/10.1002/pmic.201600053

    Article  CAS  PubMed  Google Scholar 

  32. Scheltens, P., Blennow, K., Breteler, M.M., de Strooper, B., Frisoni, G.B., Salloway, S., Van der Flier, W.M.: Alzheimer’s disease. Lancet. 388(10043), 505–517 (2016). https://doi.org/10.1016/S0140-6736(15)01124-1

    Article  CAS  PubMed  Google Scholar 

  33. Selkoe, D.J.: Resolving controversies on the path to Alzheimer’s therapeutics. Nat. Med. 17(9), 1060–1065 (2011). https://doi.org/10.1038/nm.2460

    Article  CAS  PubMed  Google Scholar 

  34. Abbott, A.: Dementia: a problem for our age. Nature. 475(7355), S2–S4 (2011). https://doi.org/10.1038/475S2a

    Article  CAS  PubMed  Google Scholar 

  35. Karran, E., Mercken, M., De Strooper, B.: The amyloid cascade hypothesis for Alzheimer’s disease: an appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 10(9), 698–712 (2011). https://doi.org/10.1038/nrd3505

    Article  CAS  PubMed  Google Scholar 

  36. Rogaev, E.I., Sherrington, R., Rogaeva, E.A., Levesque, G., Ikeda, M., Liang, Y., Chi, H., Lin, C., Holman, K., Tsuda, T., et al.: Familial Alzheimer’s disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer’s disease type 3 gene. Nature. 376(6543), 775–778 (1995). https://doi.org/10.1038/376775a0

    Article  CAS  PubMed  Google Scholar 

  37. Sherrington, R., Rogaev, E.I., Liang, Y., Rogaeva, E.A., Levesque, G., Ikeda, M., Chi, H., Lin, C., Li, G., Holman, K., Tsuda, T., Mar, L., Foncin, J.F., Bruni, A.C., Montesi, M.P., Sorbi, S., Rainero, I., Pinessi, L., Nee, L., Chumakov, I., Pollen, D., Brookes, A., Sanseau, P., Polinsky, R.J., Wasco, W., Da Silva, H.A., Haines, J.L., Perkicak-Vance, M.A., Tanzi, R.E., Roses, A.D., Fraser, P.E., Rommens, J.M., St George-Hyslop, P.H.: Cloning of a gene bearing missense mutations in early-onset familial Alzheimer’s disease. Nature. 375(6534), 754–760 (1995). https://doi.org/10.1038/375754a0

    Article  CAS  PubMed  Google Scholar 

  38. LaFerla, F.M., Green, K.N.: Animal models of Alzheimer disease. Cold Spring Harb. Perspect. Med. 2(11), (2012). https://doi.org/10.1101/cshperspect.a006320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Saito, T., Matsuba, Y., Mihira, N., Takano, J., Nilsson, P., Itohara, S., Iwata, N., Saido, T.C.: Single App knock-in mouse models of Alzheimer’s disease. Nat. Neurosci. 17(5), 661–663 (2014). https://doi.org/10.1038/nn.3697

    Article  CAS  PubMed  Google Scholar 

  40. Kizuka, Y., Kitazume, S., Taniguchi, N.: N-glycan and Alzheimer’s disease. Biochim. Biophys. Acta. 1861(10), 2447–2454 (2017). https://doi.org/10.1016/j.bbagen.2017.04.012

    Article  CAS  Google Scholar 

  41. Vassar, R., Kuhn, P.H., Haass, C., Kennedy, M.E., Rajendran, L., Wong, P.C., Lichtenthaler, S.F.: Function, therapeutic potential and cell biology of BACE proteases: current status and future prospects. J. Neurochem. 130(1), 4–28 (2014). https://doi.org/10.1111/jnc.12715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Haass, C., Kaether, C., Thinakaran, G., Sisodia, S.: Trafficking and proteolytic processing of APP. Cold Spring Harb. Perspect. Med. 2(5), a006270 (2012). https://doi.org/10.1101/cshperspect.a006270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Akasaka-Manya, K., Manya, H., Sakurai, Y., Wojczyk, B.S., Spitalnik, S.L., Endo, T.: Increased bisecting and core-fucosylated N-glycans on mutant human amyloid precursor proteins. Glycoconj. J. 25(8), 775–786 (2008). https://doi.org/10.1007/s10719-008-9140-x

    Article  CAS  PubMed  Google Scholar 

  44. Saito, F., Tani, A., Miyatake, T., Yanagisawa, K.: N-linked oligosaccharide of beta-amyloid precursor protein (beta APP) of C6 glioma cells: putative regulatory role in beta APP processing. Biochem. Biophys. Res. Commun. 210(3), 703–710 (1995). https://doi.org/10.1006/bbrc.1995.1716

    Article  CAS  PubMed  Google Scholar 

  45. Chung, H.M., Struhl, G.: Nicastrin is required for Presenilin-mediated transmembrane cleavage in drosophila. Nat. Cell Biol. 3(12), 1129–1132 (2001). https://doi.org/10.1038/ncb1201-1129

    Article  CAS  PubMed  Google Scholar 

  46. Yu, G., Nishimura, M., Arawaka, S., Levitan, D., Zhang, L., Tandon, A., Song, Y.Q., Rogaeva, E., Chen, F., Kawarai, T., Supala, A., Levesque, L., Yu, H., Yang, D.S., Holmes, E., Milman, P., Liang, Y., Zhang, D.M., Xu, D.H., Sato, C., Rogaev, E., Smith, M., Janus, C., Zhang, Y., Aebersold, R., Farrer, L.S., Sorbi, S., Bruni, A., Fraser, P., St George-Hyslop, P.: Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and betaAPP processing. Nature. 407(6800), 48–54 (2000). https://doi.org/10.1038/35024009

    Article  CAS  PubMed  Google Scholar 

  47. Kizuka, Y., Nakano, M., Kitazume, S., Saito, T., Saido, T.C., Taniguchi, N.: Bisecting GlcNAc modification stabilizes BACE1 protein under oxidative stress conditions. Biochem. J. 473(1), 21–30 (2016). https://doi.org/10.1042/BJ20150607

    Article  CAS  PubMed  Google Scholar 

  48. Kizuka, Y., Kitazume, S., Sato, K., Taniguchi, N.: Clec4g (LSECtin) interacts with BACE1 and suppresses Abeta generation. FEBS Lett. 589(13), 1418–1422 (2015). https://doi.org/10.1016/j.febslet.2015.04.060

    Article  CAS  PubMed  Google Scholar 

  49. Kurimoto, A., Kitazume, S., Kizuka, Y., Nakajima, K., Oka, R., Fujinawa, R., Korekane, H., Yamaguchi, Y., Wada, Y., Taniguchi, N.: 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. J. Biol. Chem. 289(17), 11704–11714 (2014). https://doi.org/10.1074/jbc.M113.502542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Taniguchi, N., Kizuka, Y., Takamatsu, S., Miyoshi, E., Gao, C., Suzuki, K., Kitazume, S., Ohtsubo, K.: Glyco-redox, a link between oxidative stress and changes of glycans: lessons from research on glutathione, reactive oxygen and nitrogen species to glycobiology. Arch. Biochem. Biophys. 595, 72–80 (2016). https://doi.org/10.1016/j.abb.2015.11.024

    Article  CAS  PubMed  Google Scholar 

  51. Kao, S.C., Krichevsky, A.M., Kosik, K.S., Tsai, L.H.: BACE1 suppression by RNA interference in primary cortical neurons. J. Biol. Chem. 279(3), 1942–1949 (2004). https://doi.org/10.1074/jbc.M309219200M309219200

    Article  CAS  PubMed  Google Scholar 

  52. Cheignon, C., Tomas, M., Bonnefont-Rousselot, D., Faller, P., Hureau, C., Collin, F.: Oxidative stress and the amyloid beta peptide in Alzheimer’s disease. Redox Biol. 14, 450–464 (2018). https://doi.org/10.1016/j.redox.2017.10.014

    Article  CAS  PubMed  Google Scholar 

  53. Kuhn, P.H., Koroniak, K., Hogl, S., Colombo, A., Zeitschel, U., Willem, M., Volbracht, C., Schepers, U., Imhof, A., Hoffmeister, A., Haass, C., Rossner, S., Brase, S., Lichtenthaler, S.F.: Secretome protein enrichment identifies physiological BACE1 protease substrates in neurons. EMBO J. 31(14), 3157–3168 (2012). https://doi.org/10.1038/emboj.2012.173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Zhou, L., Barao, S., Laga, M., Bockstael, K., Borgers, M., Gijsen, H., Annaert, W., Moechars, D., Mercken, M., Gevaert, K., De Strooper, B.: The neural cell adhesion molecules L1 and CHL1 are cleaved by BACE1 protease in vivo. J. Biol. Chem. 287(31), 25927–25940 (2012). https://doi.org/10.1074/jbc.M112.377465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Willem, M., Garratt, A.N., Novak, B., Citron, M., Kaufmann, S., Rittger, A., DeStrooper, B., Saftig, P., Birchmeier, C., Haass, C.: Control of peripheral nerve myelination by the beta-secretase BACE1. Science. 314(5799), 664–666 (2006). https://doi.org/10.1126/science.1132341

    Article  CAS  PubMed  Google Scholar 

  56. Hu, X., Hicks, C.W., He, W., Wong, P., Macklin, W.B., Trapp, B.D., Yan, R.: Bace1 modulates myelination in the central and peripheral nervous system. Nat. Neurosci. 9(12), 1520–1525 (2006). https://doi.org/10.1038/nn1797

    Article  CAS  PubMed  Google Scholar 

  57. Cheret, C., Willem, M., Fricker, F.R., Wende, H., Wulf-Goldenberg, A., Tahirovic, S., Nave, K.A., Saftig, P., Haass, C., Garratt, A.N., Bennett, D.L., Birchmeier, C.: Bace1 and Neuregulin-1 cooperate to control formation and maintenance of muscle spindles. EMBO J. (2013). https://doi.org/10.1038/emboj.2013.146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Dominguez, D., Tournoy, J., Hartmann, D., Huth, T., Cryns, K., Deforce, S., Serneels, L., Camacho, I.E., Marjaux, E., Craessaerts, K., Roebroek, A.J., Schwake, M., D'Hooge, R., Bach, P., Kalinke, U., Moechars, D., Alzheimer, C., Reiss, K., Saftig, P., De Strooper, B.: Phenotypic and biochemical analyses of BACE1- and BACE2-deficient mice. J. Biol. Chem. 280(35), 30797–30806 (2005). https://doi.org/10.1074/jbc.M505249200

    Article  CAS  PubMed  Google Scholar 

  59. Savonenko, A.V., Melnikova, T., Laird, F.M., Stewart, K.A., Price, D.L., Wong, P.C.: Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Proc. Natl. Acad. Sci. U. S. A. 105(14), 5585–5590 (2008). https://doi.org/10.1073/pnas.0710373105

    Article  PubMed  PubMed Central  Google Scholar 

  60. Varki, A., Cummings, R.D., Aebi, M., Packer, N.H., Seeberger, P.H., Esko, J.D., Stanley, P., Hart, G., Darvill, A., Kinoshita, T., Prestegard, J.J., Schnaar, R.L., Freeze, H.H., Marth, J.D., Bertozzi, C.R., Etzler, M.E., Frank, M., Vliegenthart, J.F., Lutteke, T., Perez, S., Bolton, E., Rudd, P., Paulson, J., Kanehisa, M., Toukach, P., Aoki-Kinoshita, K.F., Dell, A., Narimatsu, H., York, W., Taniguchi, N., Kornfeld, S.: Symbol nomenclature for graphical representations of Glycans. Glycobiology. 25(12), 1323–1324 (2015). https://doi.org/10.1093/glycob/cwv091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was partially supported by Grant-in-Aid for Scientific Research (C) to Y.K. [17 K07356], Grant-in-Aid for Challenging Exploratory Research to NT [15 K14481], Grant-in-Aid for Scientific Research (B) to NT [15H04700], Leading Initiative for Excellent Young Researchers (LEADER) project to Y.K. from the Japan Society for the Promotion of Science (JSPS), by Takeda Science Foundation, and by Mochida Memorial Foundation for Medical and Pharmaceutical Research. We thank Rebecca Porter, PhD, from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yasuhiko Kizuka or Naoyuki Taniguchi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kizuka, Y., Taniguchi, N. Neural functions of bisecting GlcNAc. Glycoconj J 35, 345–351 (2018). https://doi.org/10.1007/s10719-018-9829-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-018-9829-4

Keywords

Navigation