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Mental disorders and an acidic glycan-from the perspective of polysialic acid (PSA/polySia) and the synthesizing enzyme, ST8SIA2

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Abstract

Mental disorders, such as schizophrenia, bipolar disorder, and autism spectrum disorder, are challenging to manage, worldwide. Understanding the molecular mechanisms underlying these disorders is essential and required. Studies investigating such molecular mechanisms are well performed and important findings are accumulating apace. Based on the fact that these disorders are due in part to the accumulation of genetic and environmental risk factors, consideration of multi-molecular and/or multi-system dependent phenomena might be important. Acidic glycans are an attractive family of molecules for understanding these disorders, because impairment of the fine-tuned glycan system affects a large number of molecules that are deeply involved in normal brain function. One of the candidates of this important family of glycan epitopes in the brain is polysialic acid (PSA/polySia). PSA is a well-known molecule because of its role as an oncodevelopmental antigen and is also widely used as a marker of adult neurogenesis. Recently, several reports have suggested that PSA and PSA-related genes are associated with multiple mental disorders. The relationships among PSA, PSA-related genes, and mental disorders are reviewed here.

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References

  1. Prince, M., Patel, V., Saxena, S., Maj, M., Maselko, J., Phillips, M.R., Rahman, A.: No health without mental health. Lancet. 370, 859–877 (2007)

    Article  PubMed  Google Scholar 

  2. Foley, C., Corvin, A., Nakagome, S.: Genetics of schizophrenia: ready to translate? Curr Psychiatry Rep. 19, 61 (2017)

    Article  PubMed  Google Scholar 

  3. Tandon, R., Keshavan, M.S., Nasrallah, H.A.: Schizophrenia, "just the facts" what we know in 2008. 2. Epidemiology and etiology. Schizophr. Res. 102, 1–18 (2008)

    Article  PubMed  Google Scholar 

  4. Owen, M.J., Sawa, A., Mortensen, P.B.: Schizophrenia. Lancet. 388, 86–97 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  5. Grande, I., Berk, M., Birmaher, B., Vieta, E.: Bipolar disorder. Lancet. 387, 1561–1572 (2016)

    Article  PubMed  Google Scholar 

  6. Lai, M.C., Lombardo, M.V., Baron-Cohen, S.: Autism. Lancet. 383, 896–910 (2014)

    Article  PubMed  Google Scholar 

  7. Sato, C., Hane, M., Kitajima, K.: Relationship between ST8SIA2, polysialic acid and its binding molecules, and psychiatric disorders. Biochim. Biophys. Acta. 1860, 1739–1752 (2016)

    Article  CAS  PubMed  Google Scholar 

  8. Angata, K., Fukuda, M.: Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie. 85, 195–206 (2003)

    Article  CAS  PubMed  Google Scholar 

  9. Arai, M., Yamada, K., Toyota, T., Obata, N., Haga, S., Yoshida, Y., Nakamura, K., Minabe, Y., Ujike, H., Sora, I., Ikeda, K., Mori, N., Yoshikawa, T., Itokawa, M.: Association between polymorphisms in the promoter region of the sialyltransferase 8B (SIAT8B) gene and schizophrenia. Biol. Psychiatry. 59, 652–659 (2006)

    Article  CAS  PubMed  Google Scholar 

  10. Isomura, R., Kitajima, K., Sato, C.: Structural and functional impairments of polysialic acid by a mutated polysialyltransferase found in schizophrenia. J. Biol. Chem. 286, 21535–21545 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. McAuley, E.Z., Scimone, A., Tiwari, Y., Agahi, G., Mowry, B.J., Holliday, E.G., Donald, J.A., Weickert, C.S., Mitchell, P.B., Schofield, P.R., Fullerton, J.M.: Identification of sialyltransferase 8B as a generalized susceptibility gene for psychotic and mood disorders on chromosome 15q25-26. PLoS One. 7, e38172 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Shaw, A.D., Tiwari, Y., Kaplan, W., Heath, A., Mitchell, P.B., Schofield, P.R., Fullerton, J.M.: Characterisation of genetic variation in ST8SIA2 and its interaction region in NCAM1 in patients with bipolar disorder. PLoS One. 9, e92556 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Hane, M., Kitajima, K., Sato, C.: Effects of intronic single nucleotide polymorphisms (iSNPs) of a polysialyltransferase, ST8SIA2 gene found in psychiatric disorders on its gene products. Biochem. Biophys. Res. Commun. 478, 1123–1129 (2016)

    Article  CAS  PubMed  Google Scholar 

  14. Sato, C., Kitajima, K.: Disialic, oligosialic and polysialic acids: distribution, functions and related disease. J. Biochem. 154, 115–136 (2013)

    Article  CAS  PubMed  Google Scholar 

  15. Ono, S., Hane, M., Kitajima, K., Sato, C.: Novel regulation of fibroblast growth factor 2 (FGF2)-mediated cell growth by polysialic acid. J. Biol. Chem. 287, 3710–3722 (2012)

    Article  CAS  PubMed  Google Scholar 

  16. Seki, T.: Polysialic acid-expressing cells in adult neurogenesis. Trends Glycosci. Glycotechnol. 16, 319–330 (2004)

    Article  CAS  Google Scholar 

  17. Seki, T.: Microenvironmental elements supporting adult hippocampal neurogenesis. Anat. Sci. Int. 78, 69–78 (2003)

    Article  PubMed  Google Scholar 

  18. Seki, T., Arai, Y.: Temporal and spacial relationships between PSA-NCAM-expressing, newly generated granule cells, and radial glia-like cells in the adult dentate gyrus. J. Comp. Neurol. 410, 503–513 (1999)

    Article  CAS  PubMed  Google Scholar 

  19. Rutishauser, U.: Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26–35 (2008)

    Article  CAS  PubMed  Google Scholar 

  20. Galuska, S.P., Rollenhagen, M., Kaup, M., Eggers, K., Oltmann-Norden, I., Schiff, M., Hartmann, M., Weinhold, B., Hildebrandt, H., Geyer, R., Mühlenhoff, M., Geyer, H.: Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc. Natl. Acad. Sci. U. S. A. 107, 10250–10255 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Curreli, S., Arany, Z., Gerardy-Schahn, R., Mann, D., Stamatos, N.M.: Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. J. Biol. Chem. 282, 30346–30356 (2007)

    Article  CAS  PubMed  Google Scholar 

  22. Yabe, U., Sato, C., Matsuda, T., Kitajima, K.: Polysialic acid in human milk. CD36 is a new member of mammalian polysialic acid-containing glycoprotein. J. Biol. Chem. 278, 13875–13880 (2003)

    Article  CAS  PubMed  Google Scholar 

  23. Cremer, H., Lange, R., Christoph, A., Plomann, M., Vopper, G., Roes, J., Brown, R., Baldwin, S., Kraemer, P., Scheff, S.: Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature. 367, 455–459 (1994)

    Article  CAS  PubMed  Google Scholar 

  24. Oltmann-Norden, I., Galuska, S.P., Hildebrandt, H., Geyer, R., Gerardy-Schahn, R., Geyer, H., Mühlenhoff, M.: Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J. Biol. Chem. 283, 1463–1471 (2008)

    Article  CAS  PubMed  Google Scholar 

  25. Bonfanti, L.: PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol. 80, 129–164 (2006)

    Article  CAS  PubMed  Google Scholar 

  26. Colley, K.J., Kitajima, K., Sato, C.: Polysialic acid: biosynthesis, novel functions and applications. Crit. Rev. Biochem. Mol. Biol. 49, 498–532 (2014)

    Article  CAS  PubMed  Google Scholar 

  27. Takashima, S.: Characterization of mouse sialyltransferase genes: their evolution and diversity. Biosci. Biotechnol. Biochem. 72, 1155–1167 (2008)

    Article  CAS  PubMed  Google Scholar 

  28. Nakata, D., Zhang, L., Troy, F.A.: Molecular basis for polysialylation: a novel polybasic polysialyltransferase domain (PSTD) of 32 amino acids unique to the alpha 2,8-polysialyltransferases is essential for polysialylation. Glycoconj. J. 23, 423–436 (2006)

    Article  CAS  PubMed  Google Scholar 

  29. Foley, D., Swartzentruber, K., Colley, K.: Identification of sequences in the polysialyltransferases ST8Sia II and ST8Sia IV that are required for the protein-specific polysialylation of the neural cell adhesion molecule, NCAM. J. Biol. Chem. 284, 15505–15516 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Angata, K., Suzuki, M., Fukuda, M.: Differential and cooperative polysialylation of the neural cell adhesion molecule by two polysialyltransferases, PST and STX. J. Biol. Chem. 273, 28524–28532 (1998)

    Article  CAS  PubMed  Google Scholar 

  31. Hane, M., Matsuoka, S., Ono, S., Miyata, S., Kitajima, K., Sato, C.: Protective effects of polysialic acid on proteolytic cleavage of FGF2 and proBDNF/BDNF. Glycobiology. 25, 1112–1124 (2015)

    Article  CAS  PubMed  Google Scholar 

  32. Mori, A., Hane, M., Niimi, Y., Kitajima, K., Sato, C.: Different properties of polysialic acids synthesized by the polysialyltransferases ST8SIA2 and ST8SIA4. Glycobiology. 27, 834–846 (2017)

    Article  PubMed  Google Scholar 

  33. Angata, K., Nakayama, J., Fredette, B., Chong, K., Ranscht, B., Fukuda, M.: Human STX polysialyltransferase forms the embryonic form of the neural cell adhesion molecule. Tissue-specific expression, neurite outgrowth, and chromosomal localization in comparison with another polysialyltransferase, PST. J. Biol. Chem. 272, 7182–7190 (1997)

    Article  CAS  PubMed  Google Scholar 

  34. Yoshida, Y., Kurosawa, N., Kanematsu, T., Kojima, N., Tsuji, S.: Genomic structure and promoter activity of the mouse polysialic acid synthase gene (mST8Sia II). Brain-specific expression from a TATA-less GC-rich sequence. J. Biol. Chem. 271, 30167–30173 (1996)

    Article  CAS  PubMed  Google Scholar 

  35. Nakagawa, S., Kim, J.E., Lee, R., Chen, J., Fujioka, T., Malberg, J., Tsuji, S., Duman, R.S.: Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J. Neurosci. 22, 9868–9876 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Mayanil, C.S., George, D., Mania-Farnell, B., Bremer, C.L., McLone, D.G., Bremer, E.G.: Overexpression of murine Pax3 increases NCAM polysialylation in a human medulloblastoma cell line. J. Biol. Chem. 275, 23259–23266 (2000)

    Article  CAS  PubMed  Google Scholar 

  37. Yang, P., Yin, X., Rutishauser, U.: Intercellular space is affected by the polysialic acid content of NCAM. J. Cell Biol. 116, 1487–1496 (1992)

    Article  CAS  PubMed  Google Scholar 

  38. Hallenbeck, P., Vimr, E., Yu, F., Bassler, B., Troy, F.: Purification and properties of a bacteriophage-induced endo-N-acetylneuraminidase specific for poly-alpha-2,8-sialosyl carbohydrate units. J. Biol. Chem. 262, 3553–3561 (1987)

    CAS  PubMed  Google Scholar 

  39. Sato, C., Kitajima, K., Tazawa, I., Inoue, Y., Inoue, S., Troy, F.A.: Structural diversity in the alpha 2-->8-linked polysialic acid chains in salmonid fish egg glycoproteins. Occurrence of poly(Neu5Ac), poly(Neu5Gc), poly(Neu5Ac, Neu5Gc), poly(KDN), and their partially acetylated forms. J. Biol. Chem. 268, 23675–23684 (1993)

    CAS  PubMed  Google Scholar 

  40. Kanato, Y., Kitajima, K., Sato, C.: Direct binding of polysialic acid to a brain-derived neurotrophic factor depends on the degree of polymerization. Glycobiology. 18, 1044–1053 (2008)

    Article  CAS  PubMed  Google Scholar 

  41. Hane, M., Sumida, M., Kitajima, K., Sato, C.: Structural and functional impairments of polySia-NCAM synthesized by a mutated polysialyltransferase of a schizophrenic patient. Pure Appl. Chem. 84, 1895–1906 (2012)

    Article  CAS  Google Scholar 

  42. Buckley, P.F., Pillai, A., Howell, K.R.: Brain-derived neurotrophic factor: findings in schizophrenia. Curr. Opin. Psychiatry. 24, 122–127 (2011)

    Article  PubMed  Google Scholar 

  43. Gaughran, F., Payne, J., Sedgwick, P., Cotter, D., Berry, M.: Hippocampal FGF-2 and FGFR1 mRNA expression in major depression, schizophrenia and bipolar disorder. Brain Res. Bull. 70, 221–227 (2006)

    Article  CAS  PubMed  Google Scholar 

  44. Klejbor, I., Myers, J., Hausknecht, K., Corso, T., Gambino, A., Morys, J., Maher, P., Hard, R., Richards, J., Stachowiak, E., Stachowiak, M.: Fibroblast growth factor receptor signaling affects development and function of dopamine neurons - inhibition results in a schizophrenia-like syndrome in transgenic mice. J. Neurochem. 97, 1243–1258 (2006)

    Article  CAS  PubMed  Google Scholar 

  45. Terwisscha van Scheltinga, A.F., Bakker, S.C., Kahn, R.S.: Fibroblast growth factors in schizophrenia. Schizophr. Bull. 36, 1157–1166 (2010)

    Article  PubMed  Google Scholar 

  46. Nicodemus, K., Kolachana, B., Vakkalanka, R., Straub, R., Giegling, I., Egan, M., Rujescu, D., Weinberger, D.: Evidence for statistical epistasis between catechol-O-methyltransferase (COMT) and polymorphisms in RGS4, G72 (DAOA), GRM3, and DISC1: influence on risk of schizophrenia. Hum. Genet. 120, 889–906 (2007)

    Article  CAS  PubMed  Google Scholar 

  47. Muller, D., Djebbara-Hannas, Z., Jourdain, P., Vutskits, L., Durbec, P., Rougon, G., Kiss, J.: Brain-derived neurotrophic factor restores long-term potentiation in polysialic acid-neural cell adhesion molecule-deficient hippocampus. Proc. Natl. Acad. Sci. U. S. A. 97, 4315–4320 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sumida, M., Hane, M., Yabe, U., Shimoda, Y., Pearce, O.M.T., Kiso, M., Miyagi, T., Sawada, M., Varki, A., Kitajima, K., Sato, C.: Rapid trimming of cell surface Polysialic acid (PolySia) by exovesicular Sialidase triggers release of preexisting surface Neurotrophin. J. Biol. Chem. 290, 13202–13214 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Sato, C.: Releasing mechanism of neurotrophic factors via Polysialic acid. Vitam. Horm. 104, 89–112 (2017)

    Article  CAS  PubMed  Google Scholar 

  50. Pang, P.T., Teng, H.K., Zaitsev, E., Woo, N.T., Sakata, K., Zhen, S., Teng, K.K., Yung, W.H., Hempstead, B.L., Lu, B.: Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science. 306, 487–491 (2004)

    Article  CAS  PubMed  Google Scholar 

  51. Teng, H.K., Teng, K.K., Lee, R., Wright, S., Tevar, S., Almeida, R.D., Kermani, P., Torkin, R., Chen, Z.Y., Lee, F.S., Kraemer, R.T., Nykjaer, A., Hempstead, B.L.: ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J. Neurosci. 25, 5455–5463 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. James, W., Agnew, W.: Multiple oligosaccharide chains in the voltage-sensitive Na channel from electrophorus electricus: evidence for alpha-2,8-linked polysialic acid. Biochem. Biophys. Res. Commun. 148, 817–826 (1987)

    Article  CAS  PubMed  Google Scholar 

  53. Shimoda, Y., Kitajima, K., Inoue, S., Inoue, Y.: Calcium ion binding of three different types of oligo/polysialic acids as studied by equilibrium dialysis and circular dichroic methods. Biochemistry. 33, 1202–1208 (1994)

    Article  CAS  PubMed  Google Scholar 

  54. Vaithianathan, T., Matthias, K., Bahr, B., Schachner, M., Suppiramaniam, V., Dityatev, A., Steinhaüser, C.: Neural cell adhesion molecule-associated polysialic acid potentiates alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor Currents. J. Biol. Chem. 279, 47975–47984 (2004)

    Article  CAS  PubMed  Google Scholar 

  55. Hammond, M., Sims, C., Parameshwaran, K., Suppiramaniam, V., Schachner, M., Dityatev, A.: Neural cell adhesion molecule-associated polysialic acid inhibits NR2B-containing N-methyl-D-aspartate receptors and prevents glutamate-induced cell death. J. Biol. Chem. 281, 34859–34869 (2006)

    Article  CAS  PubMed  Google Scholar 

  56. Schnaar, R.L., Gerardy-Schahn, R., Hildebrandt, H.: Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol. Rev. 94, 461–518 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Inoko, E., Nishiura, Y., Tanaka, H., Takahashi, T., Furukawa, K., Kitajima, K., Sato, C.: Developmental stage-dependent expression of an alpha2,8-trisialic acid unit on glycoproteins in mouse brain. Glycobiology. 20, 916–928 (2010)

    Article  CAS  PubMed  Google Scholar 

  58. Galuska, S., Oltmann-Norden, I., Geyer, H., Weinhold, B., Kuchelmeister, K., Hildebrandt, H., Gerardy-Schahn, R., Geyer, R., Mühlenhoff, M.: Polysialic acid profiles of mice expressing variant allelic combinations of the polysialyltransferases ST8SiaII and ST8SiaIV. J. Biol. Chem. 281, 31605–31615 (2006)

    Article  CAS  PubMed  Google Scholar 

  59. Miragall, F., Kadmon, G., Husmann, M., Schachner, M.: Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of N-CAM. Dev. Biol. 129, 516–531 (1988)

    Article  CAS  PubMed  Google Scholar 

  60. Seki, T., Arai, Y.: The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat. Neurosci. Res. 12, 503–513 (1991)

    Article  CAS  PubMed  Google Scholar 

  61. Apple, D.M., Fonseca, R.S., Kokovay, E.: The role of adult neurogenesis in psychiatric and cognitive disorders. Brain Res. 1655, 270–276 (2017)

    Article  CAS  PubMed  Google Scholar 

  62. Oliver, P.L., Sobczyk, M.V., Maywood, E.S., Edwards, B., Lee, S., Livieratos, A., Oster, H., Butler, R., Godinho, S.I., Wulff, K., Peirson, S.N., Fisher, S.P., Chesham, J.E., Smith, J.W., Hastings, M.H., Davies, K.E., Foster, R.G.: Disrupted circadian rhythms in a mouse model of schizophrenia. Curr. Biol. 22, 314–319 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Glass, J., Watanabe, M., Fedorkova, L., Shen, H., Ungers, G., Rutishauser, U.: Dynamic regulation of polysialylated neural cell adhesion molecule in the suprachiasmatic nucleus. Neuroscience. 117, 203–211 (2003)

    Article  CAS  PubMed  Google Scholar 

  64. Landgraf, D., McCarthy, M.J., Welsh, D.K.: Circadian clock and stress interactions in the molecular biology of psychiatric disorders. Curr Psychiatry Rep. 16, 483 (2014)

    Article  PubMed  Google Scholar 

  65. Seki, T., Arai, Y.: Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat. Embryol. (Berl). 184, 395–401 (1991)

    Article  CAS  PubMed  Google Scholar 

  66. Varea, E., Castillo-Gómez, E., Gómez-Climent, M.A., Blasco-Ibáñez, J.M., Crespo, C., Martínez-Guijarro, F.J., Nàcher, J.: PSA-NCAM expression in the human prefrontal cortex. J. Chem. Neuroanat. 33, 202–209 (2007)

    Article  CAS  PubMed  Google Scholar 

  67. Nacher, J., Lanuza, E., McEwen, B.S.: Distribution of PSA-NCAM expression in the amygdala of the adult rat. Neuroscience. 113, 479–484 (2002)

    Article  CAS  PubMed  Google Scholar 

  68. Aaron, L.I., Chesselet, M.F.: Heterogeneous distribution of polysialylated neuronal-cell adhesion molecule during post-natal development and in the adult: an immunohistochemical study in the rat brain. Neuroscience. 28, 701–710 (1989)

    Article  CAS  PubMed  Google Scholar 

  69. Bonfanti, L., Olive, S., Poulain, D.A., Theodosis, D.T.: Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience. 49, 419–436 (1992)

    Article  CAS  PubMed  Google Scholar 

  70. Barbeau, D., Liang, J., Robitalille, Y., Quirion, R., Srivastava, L.: Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc. Natl. Acad. Sci. U. S. A. 92, 2785–2789 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Gilabert-Juan, J., Varea, E., Guirado, R., Blasco-Ibáñez, J.M., Crespo, C., Nácher, J.: Alterations in the expression of PSA-NCAM and synaptic proteins in the dorsolateral prefrontal cortex of psychiatric disorder patients. Neurosci. Lett. 530, 97–102 (2012)

    Article  CAS  PubMed  Google Scholar 

  72. Varea, E., Guirado, R., Gilabert-Juan, J., Martí, U., Castillo-Gomez, E., Blasco-Ibáñez, J.M., Crespo, C., Nacher, J.: Expression of PSA-NCAM and synaptic proteins in the amygdala of psychiatric disorder patients. J. Psychiatr. Res. 46, 189–197 (2012)

    Article  PubMed  Google Scholar 

  73. Lyons, F., Martin, M.L., Maguire, C., Jackson, A., Regan, C.M., Shelley, R.K.: The expression of an N-CAM serum fragment is positively correlated with severity of negative features in type II schizophrenia. Biol. Psychiatry. 23, 769–775 (1988)

    Article  CAS  PubMed  Google Scholar 

  74. Piras, F., Schiff, M., Chiapponi, C., Bossù, P., Mühlenhoff, M., Caltagirone, C., Gerardy-Schahn, R., Hildebrandt, H., Spalletta, G.: Brain structure, cognition and negative symptoms in schizophrenia are associated with serum levels of polysialic acid-modified NCAM. Transl. Psychiatry. 5, e658 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Yoshimi, K., Ren, Y., Seki, T., Yamada, M., Ooizumi, H., Onodera, M., Saito, Y., Murayama, S., Okano, H., Mizuno, Y., Mochizuki, H.: Possibility for neurogenesis in substantia nigra of parkinsonian brain. Ann. Neurol. 58, 31–40 (2005)

    Article  PubMed  Google Scholar 

  76. Murray, H.C., Low, V.F., Swanson, M.E., Dieriks, B.V., Turner, C., Faull, R.L., Curtis, M.A.: Distribution of PSA-NCAM in normal, Alzheimer's and Parkinson's disease human brain. Neuroscience. 330, 359–375 (2016)

    Article  CAS  PubMed  Google Scholar 

  77. Limón, I.D., Ramírez, E., Díaz, A., Mendieta, L., Mayoral, M., Espinosa, B., Guevara, J., Zenteno, E.: Alteration of the sialylation pattern and memory deficits by injection of Aβ(25-35) into the hippocampus of rats. Neurosci. Lett. 495, 11–16 (2011)

    Article  PubMed  CAS  Google Scholar 

  78. Tatebayashi, Y., Lee, M., Li, L., Iqbal, K., Grundke-Iqbal, I.: The dentate gyrus neurogenesis: a therapeutic target for Alzheimer's disease. Acta Neuropathol. 105, 225–232 (2003)

    CAS  PubMed  Google Scholar 

  79. Keshavan, M.S., Tandon, R., Boutros, N.N., Nasrallah, H.A.: Schizophrenia, "just the facts": what we know in 2008 part 3: neurobiology. Schizophr. Res. 106, 89–107 (2008)

    Article  PubMed  Google Scholar 

  80. Numakawa, T., Yagasaki, Y., Ishimoto, T., Okada, T., Suzuki, T., Iwata, N., Ozaki, N., Taguchi, T., Tatsumi, M., Kamijima, K., Straub, R., Weinberger, D., Kunugi, H., Hashimoto, R.: Evidence of novel neuronal functions of dysbindin, a susceptibility gene for schizophrenia. Hum. Mol. Genet. 13, 2699–2708 (2004)

    Article  CAS  PubMed  Google Scholar 

  81. Joo, E., Lee, K., Jeong, S., Roh, M., Kim, S., Ahn, Y., Kim, Y.: AKT1 gene polymorphisms and obstetric complications in the patients with schizophrenia. Psychiatry Investig. 6, 102–107 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Allen, N., Bagade, S., McQueen, M., Ioannidis, J., Kavvoura, F., Khoury, M., Tanzi, R., Bertram, L.: Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: the SzGene database. Nat. Genet. 40, 827–834 (2008)

    Article  CAS  PubMed  Google Scholar 

  83. Devon, R., Anderson, S., Teague, P., Burgess, P., Kipari, T., Semple, C., Millar, J., Muir, W., Murray, V., Pelosi, A., Blackwood, D., Porteous, D.: Identification of polymorphisms within disrupted in schizophrenia 1 and disrupted in schizophrenia 2, and an investigation of their association with schizophrenia and bipolar affective disorder. Psychiatr. Genet. 11, 71–78 (2001)

    Article  CAS  PubMed  Google Scholar 

  84. Kamiya, A., Tomoda, T., Chang, J., Takaki, M., Zhan, C., Morita, M., Cascio, M., Elashvili, S., Koizumi, H., Takanezawa, Y., Dickerson, F., Yolken, R., Arai, H., Sawa, A.: DISC1-NDEL1/NUDEL protein interaction, an essential component for neurite outgrowth, is modulated by genetic variations of DISC1. Hum. Mol. Genet. 15, 3313–3323 (2006)

    Article  CAS  PubMed  Google Scholar 

  85. Taya, S., Shinoda, T., Tsuboi, D., Asaki, J., Nagai, K., Hikita, T., Kuroda, S., Kuroda, K., Shimizu, M., Hirotsune, S., Iwamatsu, A., Kaibuchi, K.: DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J. Neurosci. 27, 15–26 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Stefansson, H., Sigurdsson, E., Steinthorsdottir, V., Bjornsdottir, S., Sigmundsson, T., Ghosh, S., Brynjolfsson, J., Gunnarsdottir, S., Ivarsson, O., Chou, T.T., Hjaltason, O., Birgisdottir, B., Jonsson, H., Gudnadottir, V.G., Gudmundsdottir, E., Bjornsson, A., Ingvarsson, B., Ingason, A., Sigfusson, S., Hardardottir, H., Harvey, R.P., Lai, D., Zhou, M., Brunner, D., Mutel, V., Gonzalo, A., Lemke, G., Sainz, J., Johannesson, G., Andresson, T., Gudbjartsson, D., Manolescu, A., Frigge, M.L., Gurney, M.E., Kong, A., Gulcher, J.R., Petursson, H., Stefansson, K.: Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71, 877–892 (2002)

    Article  PubMed  PubMed Central  Google Scholar 

  87. Akbarian, S., Huang, H.S.: Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders. Brain Res. Rev. 52, 293–304 (2006)

    Article  CAS  PubMed  Google Scholar 

  88. Craddock, N., O'Donovan, M., Owen, M.: The genetics of schizophrenia and bipolar disorder: dissecting psychosis. J. Med. Genet. 42, 193–204 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Barnett, J., Smoller, J.: The genetics of bipolar disorder. Neuroscience. 164, 331–343 (2009)

    Article  CAS  PubMed  Google Scholar 

  90. Jiang, Y.H., Ehlers, M.D.: Modeling autism by SHANK gene mutations in mice. Neuron. 78, 8–27 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Zhiling, Y., Fujita, E., Tanabe, Y., Yamagata, T., Momoi, T., Momoi, M.Y.: Mutations in the gene encoding CADM1 are associated with autism spectrum disorder. Biochem. Biophys. Res. Commun. 377, 926–929 (2008)

    Article  CAS  PubMed  Google Scholar 

  92. Wilkinson, B., Grepo, N., Thompson, B.L., Kim, J., Wang, K., Evgrafov, O.V., Lu, W., Knowles, J.A., Campbell, D.B.: The autism-associated gene chromodomain helicase DNA-binding protein 8 (CHD8) regulates noncoding RNAs and autism-related genes. Transl. Psychiatry. 5, e568 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Maziade, M., Roy, M., Chagnon, Y., Cliche, D., Fournier, J., Montgrain, N., Dion, C., Lavallée, J., Garneau, Y., Gingras, N., Nicole, L., Pirès, A., Ponton, A., Potvin, A., Wallot, H., Mérette, C.: Shared and specific susceptibility loci for schizophrenia and bipolar disorder: a dense genome scan in eastern Quebec families. Mol. Psychiatry. 10, 486–499 (2005)

    Article  CAS  PubMed  Google Scholar 

  94. Brocco, M., Pollevick, G.D., Frasch, A.C.: Differential regulation of polysialyltransferase expression during hippocampus development: implications for neuronal survival. J. Neurosci. Res. 74, 744–753 (2003)

    Article  CAS  PubMed  Google Scholar 

  95. Tao, R., Li, C., Zheng, Y., Qin, W., Zhang, J., Li, X., Xu, Y., Shi, Y.Y., Feng, G., He, L.: Positive association between SIAT8B and schizophrenia in the Chinese Han population. Schizophr. Res. 90, 108–114 (2007)

    Article  PubMed  Google Scholar 

  96. Gilabert-Juan, J., Nacher, J., Sanjuán, J., Moltó, M.D.: Sex-specific association of the ST8SIAII gene with schizophrenia in a Spanish population. Psychiatry Res. 210, 1293–1295 (2013)

    Article  CAS  PubMed  Google Scholar 

  97. Yang, S.Y., Huh, I.S., Baek, J.H., Cho, E.Y., Choi, M.J., Ryu, S., Kim, J.S., Park, T., Ha, K., Hong, K.S.: Association between ST8SIA2 and the risk of schizophrenia and bipolar I disorder across diagnostic boundaries. PLoS One. 10, e0139413 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Fullerton, J.M., Klauser, P., Lenroot, R.K., Shaw, A.D., Overs, B., Heath, A., Cairns, M.J., Atkins, J., Scott, R., Schofield, P.R., Weickert, C.S., Pantelis, C., Fornito, A., Whitford, T.J., Weickert, T.W., Zalesky, A., Bank, A.S.R.: Differential effect of disease-associated ST8SIA2 haplotype on cerebral white matter diffusion properties in schizophrenia and healthy controls. Transl. Psychiatry. 8, 21 (2018)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Arai, M., Itokawa, M., Yamada, K., Toyota, T., Haga, S., Ujike, H., Sora, I., Ikeda, K., Yoshikawa, T.: Association of neural cell adhesion molecule 1 gene polymorphisms with bipolar affective disorder in Japanese individuals. Biol. Psychiatry. 55, 804–810 (2004)

    Article  CAS  PubMed  Google Scholar 

  100. Park, N., Juo, S.H., Cheng, R., Liu, J., Loth, J.E., Lilliston, B., Nee, J., Grunn, A., Kanyas, K., Lerer, B., Endicott, J., Gilliam, T.C., Baron, M.: Linkage analysis of psychosis in bipolar pedigrees suggests novel putative loci for bipolar disorder and shared susceptibility with schizophrenia. Mol. Psychiatry. 9, 1091–1099 (2004)

    Article  CAS  PubMed  Google Scholar 

  101. Lee, M.T., Chen, C.H., Lee, C.S., Chen, C.C., Chong, M.Y., Ouyang, W.C., Chiu, N.Y., Chuo, L.J., Chen, C.Y., Tan, H.K., Lane, H.Y., Chang, T.J., Lin, C.H., Jou, S.H., Hou, Y.M., Feng, J., Lai, T.J., Tung, C.L., Chen, T.J., Chang, C.J., Lung, F.W., Chen, C.K., Shiah, I.S., Liu, C.Y., Teng, P.R., Chen, K.H., Shen, L.J., Cheng, C.S., Chang, T.P., Li, C.F., Chou, C.H., Wang, K.H., Fann, C.S., Wu, J.Y., Chen, Y.T., Cheng, A.T.: Genome-wide association study of bipolar I disorder in the Han Chinese population. Mol. Psychiatry. 16, 548–556 (2011)

    Article  CAS  PubMed  Google Scholar 

  102. Yang, S.Y., Baek, J.H., Cho, Y., Cho, E.Y., Choi, Y., Kim, Y., Park, T., Hong, K.S.: Effects of genetic variants of ST8SIA2 and NCAM1 genes on seasonal mood changes and circadian preference in the general Population. Chronobiol. Int. 35, 405–415 (2018)

    Article  CAS  PubMed  Google Scholar 

  103. Anney, R., Klei, L., Pinto, D., Regan, R., Conroy, J., Magalhaes, T.R., Correia, C., Abrahams, B.S., Sykes, N., Pagnamenta, A.T., Almeida, J., Bacchelli, E., Bailey, A.J., Baird, G., Battaglia, A., Berney, T., Bolshakova, N., Bölte, S., Bolton, P.F., Bourgeron, T., Brennan, S., Brian, J., Carson, A.R., Casallo, G., Casey, J., Chu, S.H., Cochrane, L., Corsello, C., Crawford, E.L., Crossett, A., Dawson, G., de Jonge, M., Delorme, R., Drmic, I., Duketis, E., Duque, F., Estes, A., Farrar, P., Fernandez, B.A., Folstein, S.E., Fombonne, E., Freitag, C.M., Gilbert, J., Gillberg, C., Glessner, J.T., Goldberg, J., Green, J., Guter, S.J., Hakonarson, H., Heron, E.A., Hill, M., Holt, R., Howe, J.L., Hughes, G., Hus, V., Igliozzi, R., Kim, C., Klauck, S.M., Kolevzon, A., Korvatska, O., Kustanovich, V., Lajonchere, C.M., Lamb, J.A., Laskawiec, M., Leboyer, M., Le Couteur, A., Leventhal, B.L., Lionel, A.C., Liu, X.Q., Lord, C., Lotspeich, L., Lund, S.C., Maestrini, E., Mahoney, W., Mantoulan, C., Marshall, C.R., McConachie, H., McDougle, C.J., McGrath, J., McMahon, W.M., Melhem, N.M., Merikangas, A., Migita, O., Minshew, N.J., Mirza, G.K., Munson, J., Nelson, S.F., Noakes, C., Noor, A., Nygren, G., Oliveira, G., Papanikolaou, K., Parr, J.R., Parrini, B., Paton, T., Pickles, A., Piven, J., Posey, D.J., Poustka, A., Poustka, F., Prasad, A., Ragoussis, J., Renshaw, K., Rickaby, J., Roberts, W., Roeder, K., Roge, B., Rutter, M.L., Bierut, L.J., Rice, J.P., Salt, J., Sansom, K., Sato, D., Segurado, R., Senman, L., Shah, N., Sheffield, V.C., Soorya, L., Sousa, I., Stoppioni, V., Strawbridge, C., Tancredi, R., Tansey, K., Thiruvahindrapduram, B., Thompson, A.P., Thomson, S., Tryfon, A., Tsiantis, J., Van Engeland, H., Vincent, J.B., Volkmar, F., Wallace, S., Wang, K., Wang, Z., Wassink, T.H., Wing, K., Wittemeyer, K., Wood, S., Yaspan, B.L., Zurawiecki, D., Zwaigenbaum, L., Betancur, C., Buxbaum, J.D., Cantor, R.M., Cook, E.H., Coon, H., Cuccaro, M.L., Gallagher, L., Geschwind, D.H., Gill, M., Haines, J.L., Miller, J., Monaco, A.P., Nurnberger, J.I., Paterson, A.D., Pericak-Vance, M.A., Schellenberg, G.D., Scherer, S.W., Sutcliffe, J.S., Szatmari, P., Vicente, A.M., Vieland, V.J., Wijsman, E.M., Devlin, B., Ennis, S., Hallmayer, J.: A genome-wide scan for common alleles affecting risk for autism. Hum. Mol. Genet. 19, 4072–4082 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Kamien, B., Harraway, J., Lundie, B., Smallhorne, L., Gibbs, V., Heath, A., Fullerton, J.M.: Characterization of a 520 kb deletion on chromosome 15q26.1 including ST8SIA2 in a patient with behavioral disturbance, autism spectrum disorder, and epilepsy. Am. J. Med. Genet. A. 164A, 782–788 (2014)

    Article  PubMed  CAS  Google Scholar 

  105. Kamien, B., Harraway, J., Lundie, B., Smallhorne, L., Gibbs, V., Heath, A., Fullerton, J.M.: Characterization of a 520 kb deletion on chromosome 15q26.1 including ST8SIA2 in a patient with behavioral disturbance, autism spectrum disorder, and epilepsy: additional information. Am. J. Med. Genet. A. 167, 1424 (2015)

    Article  PubMed  Google Scholar 

  106. Fatemi, S.H., King, D.P., Reutiman, T.J., Folsom, T.D., Laurence, J.A., Lee, S., Fan, Y.T., Paciga, S.A., Conti, M., Menniti, F.S.: PDE4B polymorphisms and decreased PDE4B expression are associated with schizophrenia. Schizophr. Res. 101, 36–49 (2008)

    Article  PubMed  Google Scholar 

  107. Sato, C., Hirabayashi, J.: Frontal affinity chromatography: practice of weak interaction analysis between lectins and fluorescently labeled oligosaccharides. Lectins: Methods and Protocols. 1200, 257–264 (2014)

    CAS  Google Scholar 

  108. Gilabert-Juan, J., Belles, M., Saez, A.R., Carceller, H., Zamarbide-Fores, S., Moltó, M.D., Nacher, J.: A "double hit" murine model for schizophrenia shows alterations in the structure and neurochemistry of the medial prefrontal cortex and the hippocampus. Neurobiol. Dis. 59, 126–140 (2013)

    Article  CAS  PubMed  Google Scholar 

  109. Castillo-Gómez, E., Pérez-Rando, M., Bellés, M., Gilabert-Juan, J., Llorens, J. V., Carceller, H., Bueno-Fernández, C., García-Mompó, C., Ripoll-Martínez, B., Curto, Y., Sebastiá-Ortega, N., Moltó, M. D., Sanjuan, J., Nacher, J.: Early social isolation stress and perinatal NMDA receptor antagonist treatment induce changes in the structure and neurochemistry of inhibitory neurons of the adult amygdala and prefrontal cortex. eNeuro. 10, 1523 (2017)

  110. Abe, C., Nishimura, S., Mori, A., Niimi, Y., Yang, Y., Hane, M., Kitajima, K., Sato, C.: Chlorpromazine increases the expression of Polysialic acid (PolySia) in human neuroblastoma cells and mouse prefrontal cortex. Int. J. Mol. Sci. 18, (2017)

    Article  PubMed Central  Google Scholar 

  111. Miyamoto, S., Miyake, N., Jarskog, L.F., Fleischhacker, W.W., Lieberman, J.A.: Pharmacological treatment of schizophrenia: a critical review of the pharmacology and clinical effects of current and future therapeutic agents. Mol. Psychiatry. 17, 1206–1227 (2012)

    Article  CAS  PubMed  Google Scholar 

  112. Subtil, A., Hémar, A., Dautry-Varsat, A.: Rapid endocytosis of interleukin 2 receptors when clathrin-coated pit endocytosis is inhibited. J. Cell Sci. 107(Pt 12), 3461–3468 (1994)

    CAS  PubMed  Google Scholar 

  113. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Gerardy-Schahn, R., Cremer, H., Dityatev, A.: Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J. Neurosci. 20, 5234–5244 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Zerwas, M., Trouche, S., Richetin, K., Escudé, T., Halley, H., Gerardy-Schahn, R., Verret, L., Rampon, C.: Environmental enrichment rescues memory in mice deficient for the polysialytransferase ST8SiaIV. Brain Struct. Funct. 221, 1591–1605 (2016)

    Article  CAS  PubMed  Google Scholar 

  115. Tomasiewicz, H., Ono, K., Yee, D., Thompson, C., Goridis, C., Rutishauser, U., Magnuson, T.: Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron. 11, 1163–1174 (1993)

    Article  CAS  PubMed  Google Scholar 

  116. Angata, K., Long, J.M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A., Schachner, M., Fukuda, M., Marth, J.D.: Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J. Biol. Chem. 279, 32603–32613 (2004)

    Article  CAS  PubMed  Google Scholar 

  117. Weinhold, B., Seidenfaden, R., Röckle, I., Mühlenhoff, M., Schertzinger, F., Conzelmann, S., Marth, J.D., Gerardy-Schahn, R., Hildebrandt, H.: Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem. 280, 42971–42977 (2005)

    Article  CAS  PubMed  Google Scholar 

  118. Hildebrandt, H., Mühlenhoff, M., Oltmann-Norden, I., Röckle, I., Burkhardt, H., Weinhold, B., Gerardy-Schahn, R.: Imbalance of neural cell adhesion molecule and polysialyltransferase alleles causes defective brain connectivity. Brain. 132, 2831–2838 (2009)

    Article  PubMed  Google Scholar 

  119. Turetsky, B.I., Moberg, P.J., Yousem, D.M., Doty, R.L., Arnold, S.E., Gur, R.E.: Reduced olfactory bulb volume in patients with schizophrenia. Am. J. Psychiatry. 157, 828–830 (2000)

    Article  CAS  PubMed  Google Scholar 

  120. Turetsky, B.I., Moberg, P.J., Arnold, S.E., Doty, R.L., Gur, R.E.: Low olfactory bulb volume in first-degree relatives of patients with schizophrenia. Am. J. Psychiatry. 160, 703–708 (2003)

    Article  PubMed  Google Scholar 

  121. Tamminga, C.A., Stan, A.D., Wagner, A.D.: The hippocampal formation in schizophrenia. Am. J. Psychiatry. 167, 1178–1193 (2010)

    Article  PubMed  Google Scholar 

  122. Seki, T., Rutishauser, U.: Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J. Neurosci. 18, 3757–3766 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kröcher, T., Malinovskaja, K., Jürgenson, M., Aonurm-Helm, A., Zharkovskaya, T., Kalda, A., Röckle, I., Schiff, M., Weinhold, B., Gerardy-Schahn, R., Hildebrandt, H., Zharkovsky, A.: Schizophrenia-like phenotype of polysialyltransferase ST8SIA2-deficient mice. Brain Struct. Funct. (2013)

  124. Brugger, S.P., Howes, O.D.: Heterogeneity and homogeneity of regional brain structure in schizophrenia: a meta-analysis. JAMA Psychiatry. 74, 1104–1111 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  125. Shen, H., Watanabe, M., Tomasiewicz, H., Glass, J.: Genetic deletions of NCAM and PSA impair circadian function in the mouse. Physiol. Behav. 73, 185–193 (2001)

    Article  CAS  PubMed  Google Scholar 

  126. Calandreau, L., Márquez, C., Bisaz, R., Fantin, M., Sandi, C.: Differential impact of polysialyltransferase ST8SiaII and ST8SiaIV knockout on social interaction and aggression. Genes Brain Behav. 9, 958–967 (2010)

    Article  CAS  PubMed  Google Scholar 

  127. Albrecht, A., Stork, O.: Are NCAM deficient mice an animal model for schizophrenia? Front. Behav. Neurosci. 6, 43 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  128. Sato, C., Kitajima, K., Inoue, S., Seki, T., Troy, F.A., Inoue, Y.: Characterization of the antigenic specificity of four different anti-(alpha 2-->8-linked polysialic acid) antibodies using lipid-conjugated oligo/polysialic acids. J. Biol. Chem. 270, 18923–18928 (1995)

    Article  CAS  PubMed  Google Scholar 

  129. Irie, F., Badie-Mahdavi, H., Yamaguchi, Y.: Autism-like socio-communicative deficits and stereotypies in mice lacking heparan sulfate. Proc. Natl. Acad. Sci. U. S. A. 109, 5052–5056 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Kanato, Y., Ono, S., Kitajima, K., Sato, C.: Complex formation of a brain-derived neurotrophic factor and glycosaminoglycans. Biosci. Biotechnol. Biochem. 73, 2735–2741 (2009)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This review was supported in part by the DAIKO foundation (CS) and Mizutani Foundation (CS).

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  1. Bioscience and Biotechnolgy Center, Laboratory of Animal Cell Function, Nagoya University, Nagoya, 464-8601, Japan

    Chihiro Sato & Masaya Hane

  2. Department of Cellular & Molecular Medicine, UCSD, La Jolla, 92093-0687, USA

    Masaya Hane

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  1. Chihiro Sato
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Sato, C., Hane, M. Mental disorders and an acidic glycan-from the perspective of polysialic acid (PSA/polySia) and the synthesizing enzyme, ST8SIA2. Glycoconj J 35, 353–373 (2018). https://doi.org/10.1007/s10719-018-9832-9

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