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2015 | OriginalPaper | Chapter

Polysialic Acid in Brain Development and Synaptic Plasticity

Authors : Herbert Hildebrandt, Alexander Dityatev

Published in: SialoGlyco Chemistry and Biology I

Publisher: Springer Berlin Heidelberg

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Abstract

Polymers of sialic acid can be produced by pro- and eukaryotic cells. In vertebrates polysialic acid consists of α2,8-linked N-acetylneuraminic acid and is most prominent during nervous system development. Polysialic acid is produced by two complementary sialyltransferases, ST8SiaII and ST8SiaIV. The major, but not the only, carrier of polysialic acid is the neural cell adhesion molecule (NCAM). In this review we highlight how polySia dictates the interactions of various cell types during development and plasticity of the vertebrate central nervous system on different molecular levels. Recent progress in generating mouse models with differential ablation of the polysialyltransferases or NCAM revealed the dramatic impact of polysialic acid-negative NCAM on brain development and elaborate electrophysiological studies allowed for new insights into the role of polysialic acid in regulating synaptic plasticity and learning. The implications of dysregulated polysialylation for brain disease and neuropsychiatric disorders are discussed.

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previous chapter Why Is N-Glycolylneuraminic Acid Rare in the Vertebrate Brain?

next chapter UDP-GlcNAc 2-Epimerase/ManNAc Kinase (GNE): A Master Regulator of Sialic Acid Synthesis

The most commonly used abbreviation for polysialic acid in neuroscience is PSA but in tumor biology, PSA stands for prostate specific antigen. To avoid confusion we prefer to use polySia to abbreviate polysialic acid.

Jakobsson E, Schwarzer D, Jokilammi A et al (2012) Endosialidases: versatile tools for the study of polysialic acid. Top Curr Chem. doi:10.1007/128_2012_349 (e-pub ahead of print)

Troy FA (1992) Polysialylation: from bacteria to brains. Glycobiology 2:5–23

Mühlenhoff M, Eckhardt M, Gerardy-Schahn R (1998) Polysialic acid: three-dimensional structure, biosynthesis and function. Curr Opin Struct Biol 8:558–564

Finne J (1982) Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J Biol Chem 257:11966–11970

Galuska SP, Geyer R, Gerardy-Schahn R et al (2008) Enzyme-dependent variations in the polysialylation of the neural cell adhesion molecule (NCAM) in vivo. J Biol Chem 283:17–28

Brisson JR, Baumann H, Imberty A et al (1992) Helical epitope of the group B meningococcal alpha(2–8)-linked sialic acid polysaccharide. Biochemistry 31:4996–5004

Baumann H, Brisson JR, Michon F et al (1993) Comparison of the conformation of the epitope of alpha (2–>8) polysialic acid with its reduced and N-acyl derivatives. Biochemistry 32:4007–4013

Evans SV, Sigurskjold BW, Jennings HJ et al (1995) Evidence for the extended helical nature of polysaccharide epitopes. The 2.8 A resolution structure and thermodynamics of ligand binding of an antigen binding fragment specific for alpha-(2–>8)-polysialic acid. Biochemistry 34:6737–6744

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

10.

Fujimoto I, Bruses JL, Rutishauser U (2001) Regulation of cell adhesion by polysialic acid: effects on cadherin, IgCAM and integrin function and independence from NCAM binding or signaling activity. J Biol Chem 276:31745–31751

11.

Johnson CP, Fragneto G, Konovalov O et al (2005) Structural studies of the neural-cell-adhesion molecule by X-ray and neutron reflectivity. Biochemistry 44:546–554

12.

Johnson CP, Fujimoto I, Rutishauser U et al (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 280:137–145

13.

Jorgensen OS, Bock E (1974) Brain specific synaptosomal membrane proteins demonstrated by crossed immunoelectrophoresis. J Neurochem 23:879–880

14.

Edelman GM, Chuong CM (1982) Embryonic to adult conversion of neural cell adhesion molecules in normal and staggerer mice. Proc Natl Acad Sci USA 79:7036–7040

15.

Rothbard JB, Brackenbury R, Cunningham BA et al (1982) Differences in the carbohydrate structures of neural cell-adhesion molecules from adult and embryonic chicken brains. J Biol Chem 257:11064–11069

16.

Finne J, Finne U, Deagostini-Bazin H et al (1983) Occurrence of alpha 2–8 linked polysialosyl units in a neural cell adhesion molecule. Biochem Biophys Res Commun 112:482–487

17.

Sadoul R, Hirn M, Deagostini-Bazin H et al (1983) Adult and embryonic mouse neural cell adhesion molecules have different binding properties. Nature 304:347–349

18.

Hoffman S, Edelman GM (1983) Kinetics of homophilic binding by embryonic and adult forms of neural cell adhesion molecule. Proc Natl Acad Sci USA 80:5762–5766

19.

Rutishauser U, Watanabe M, Silver J et al (1985) Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol 101:1842–1849

20.

Rutishauser U, Acheson A, Hall AK et al (1988) The neural cell adhesion molecule (NCAM) as a regulator of cell–cell interactions. Science 240:53–57

21.

Seidenfaden R, Krauter A, Schertzinger F et al (2003) Polysialic acid directs tumor cell growth by controlling heterophilic neural cell adhesion molecule interactions. Mol Cell Biol 23:5908–5918

22.

Seidenfaden R, Krauter A, Hildebrandt H (2006) The neural cell adhesion molecule NCAM regulates neuritogenesis by multiple mechanisms of interaction. Neurochem Int 49:1–11

23.

Eggers K, Werneburg S, Schertzinger A et al (2011) Polysialic acid controls NCAM signals at cell–cell contacts to regulate focal adhesion independent from FGF receptor activity. J Cell Sci 124:3279–3291

24.

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

25.

Curreli S, Arany Z, Gerardy-Schahn R et al (2007) 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

26.

Rey-Gallardo A, Escribano C, Delgado-Martin C et al (2010) Polysialylated neuropilin-2 enhances human dendritic cell migration through the basic C-terminal region of CCL21. Glycobiology 20:1139–1146

27.

Rey-Gallardo A, Delgado-Martin C, Gerardy-Schahn R et al (2011) Polysialic acid is required for neuropilin-2a/b-mediated control of CCL21-driven chemotaxis of mature dendritic cells and for their migration in vivo. Glycobiology 21:655–662

28.

Mühlenhoff M, Eckhardt M, Bethe A et al (1996) Autocatalytic polysialylation of polysialyltransferase-1. EMBO J 15:6943–6950

29.

Close BE, Colley KJ (1998) In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J Biol Chem 273:34586–34593

30.

Close BE, Tao K, Colley KJ (2000) Polysialyltransferase-1 autopolysialylation is not requisite for polysialylation of neural cell adhesion molecule. J Biol Chem 275:4484–4491

31.

Close BE, Wilkinson JM, Bohrer TJ et al (2001) The polysialyltransferase ST8Sia II/STX: posttranslational processing and role of autopolysialylation in the polysialylation of neural cell adhesion molecule. Glycobiology 11:997–1008

32.

Zuber C, Lackie PM, Catterall WA et al (1992) Polysialic acid is associated with sodium channels and the neural cell adhesion molecule N-CAM in adult rat brain. J Biol Chem 267:9965–9971

33.

Galuska SP, Rollenhagen M, Kaup M et al (2010) Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc Natl Acad Sci USA 107:10250–10255

34.

Eckhardt M, Mühlenhoff M, Bethe A et al (1995) Molecular characterization of eukaryotic polysialyltransferase-1. Nature 373:715–718

35.

Nakayama J, Fukuda MN, Fredette B et al (1995) Expression cloning of a human polysialyltransferase that forms the polysialylated neural cell adhesion molecule present in embryonic brain. Proc Natl Acad Sci USA 92:7031–7035

36.

Kojima N, Yoshida Y, Tsuji S (1995) A developmentally regulated member of the sialyltransferase family (ST8Sia II, STX) is a polysialic acid synthase. FEBS Lett 373:119–122

37.

Scheidegger EP, Sternberg LR, Roth J et al (1995) A human STX cDNA confers polysialic acid expression in mammalian cells. J Biol Chem 270:22685–22688

38.

Livingston BD, Paulson JC (1993) Polymerase chain reaction cloning of a developmentally regulated member of the sialyltransferase gene family. J Biol Chem 268:11504–11507

39.

Tsuji S, Datta AK, Paulson JC (1996) Systematic nomenclature for sialyltransferases. Glycobiology 6:R5–R7

40.

Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA et al (2001) The human sialyltransferase family. Biochimie 83:727–737

41.

Harduin-Lepers A, Mollicone R, Delannoy P et al (2005) The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology 15:805–817

42.

Datta AK, Paulson JC (1995) The sialyltransferase “sialylmotif” participates in binding the donor substrate CMP-NeuAc. J Biol Chem 270:1497–1500

43.

Datta AK, Sinha A, Paulson JC (1998) Mutation of the sialyltransferase S-sialylmotif alters the kinetics of the donor and acceptor substrates. J Biol Chem 273:9608–9614

44.

Nakata D, Zhang L, Troy FA (2006) 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

45.

Foley DA, Swartzentruber KG, Colley KJ (2009) 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

46.

Zapater JL, Colley KJ (2012) Sequences prior to conserved catalytic motifs of the polysialyltransferase, ST8SiaIV, are required for substrate recognition. J Biol Chem 287:6441–6453

47.

Windfuhr M, Manegold A, Mühlenhoff M et al (2000) Molecular defects that cause loss of polysialic acid in the complementation group 2A10. J Biol Chem 275:32861–32870

48.

Mühlenhoff M, Manegold A, Windfuhr M et al (2001) The impact of N-glycosylation on the functions of polysialyltransferases. J Biol Chem 276:34066–34073

49.

Münster-Kühnel AK, Tiralongo J, Krapp S et al (2004) Structure and function of vertebrate CMP-sialic acid synthetases. Glycobiology 14:43R–51R

50.

Kudo M, Kitajima K, Inoue S et al (1996) Characterization of the major core structures of the alpha 2–>8-linked polysialic acid-containing glycan chains present in neural cell adhesion molecule in embryonic chick brains. J Biol Chem 271:32667–32677

51.

Geyer H, Bahr U, Liedtke S et al (2001) Core structures of polysialylated glycans present in neural cell adhesion molecule from newborn mouse brain. Eur J Biochem 268:6587–6599

52.

Liedtke S, Geyer H, Wuhrer M et al (2001) Characterization of N-glycans from mouse brain neural cell adhesion molecule. Glycobiology 11:373–384

53.

von der Ohe M, Wheeler SF, Wuhrer M et al (2002) Localization and characterization of polysialic acid-containing N-linked glycans from bovine NCAM. Glycobiology 12:47–63

54.

Wuhrer M, Geyer H, von der Ohe M et al (2003) Localization of defined carbohydrate epitopes in bovine polysialylated NCAM. Biochimie 85:207–218

55.

Mühlenhoff M, Eckhardt M, Bethe A et al (1996) Polysialylation of NCAM by a single enzyme. Curr Biol 6:1188–1191

56.

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

57.

Nelson RW, Bates PA, Rutishauser U (1995) Protein determinants for specific polysialylation of the neural cell adhesion molecule. J Biol Chem 270:17171–17179

58.

Colley KJ (2010) Structural basis for the polysialylation of the neural cell adhesion molecule. Adv Exp Med Biol 663:111–126

59.

Foley DA, Swartzentruber KG, Lavie A et al (2010) Structure and mutagenesis of neural cell adhesion molecule domains: evidence for flexibility in the placement of polysialic acid attachment sites. J Biol Chem 285:27360–27371

60.

Thompson MG, Foley DA, Swartzentruber KG et al (2011) Sequences at the interface of the fifth immunoglobulin domain and first fibronectin type III repeat of the neural cell adhesion molecule are critical for its polysialylation. J Biol Chem 286:4525–4534

61.

Park TU, Lucka L, Reutter W et al (1997) Turnover studies of the neural cell adhesion molecule NCAM: degradation of NCAM in PC12 cells depends on the presence of NGF. Biochem Biophys Res Commun 234:686–689

62.

Minana R, Duran JM, Tomas M et al (2001) Neural cell adhesion molecule is endocytosed via a clathrin-dependent pathway. Eur J Neurosci 13:749–756

63.

Diestel S, Schaefer D, Cremer H et al (2007) NCAM is ubiquitylated, endocytosed and recycled in neurons. J Cell Sci 120:4035–4049

64.

Schiff M, Weinhold B, Grothe C et al (2009) NCAM and polysialyltransferase profiles match dopaminergic marker gene expression but polysialic acid is dispensable for development of the midbrain dopamine system. J Neurochem 110:1661–1673

65.

Galuska SP, Oltmann-Norden I, Geyer H et al (2006) Polysialic acid profiles of mice expressing variant allelic combinations of the polysialyltransferases ST8SiaII and ST8SiaIV. J Biol Chem 281:31605–31615

66.

Oltmann-Norden I, Galuska SP, Hildebrandt H et al (2008) Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J Biol Chem 283:1463–1471

67.

Probstmeier R, Bilz A, Schneider-Schaulies J (1994) Expression of the neural cell adhesion molecule and polysialic acid during early mouse embryogenesis. J Neurosci Res 37:324–335

68.

Ong E, Nakayama J, Angata K et al (1998) Developmental regulation of polysialic acid synthesis in mouse directed by two polysialyltransferases, PST and STX. Glycobiology 8:415–424

69.

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

70.

Li H, Babiarz J, Woodbury J et al (2004) Spatiotemporal heterogeneity of CNS radial glial cells and their transition to restricted precursors. Dev Biol 271:225–238

71.

Hekmat A, Bitter-Suermann D, Schachner M (1990) Immunocytological localization of the highly polysialylated form of the neural cell adhesion molecule during development of the murine cerebellar cortex. J Comp Neurol 291:457–467

72.

Bartsch U, Kirchhoff F, Schachner M (1990) Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J Neurocytol 19:550–565

73.

Kustermann S, Hildebrandt H, Bolz S et al (2010) Genesis of rods in the zebrafish retina occurs in a microenvironment provided by polysialic acid-expressing Muller glia. J Comp Neurol 518:636–646

74.

Bonfanti L, Theodosis DT (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 62:291–305

75.

Rousselot P, Nottebohm F (1995) Expression of polysialylated N-CAM in the central nervous system of adult canaries and its possible relation to function. J Comp Neurol 356:629–640

76.

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

77.

Seki T, Arai Y (1993) Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci Res 17:265–290

78.

Chung KY, Leung KM, Lin CC et al (2004) Regionally specific expression of L1 and sialylated NCAM in the retinofugal pathway of mouse embryos. J Comp Neurol 471:482–498

79.

Daston MM, Bastmeyer M, Rutishauser U et al (1996) Spatially restricted increase in polysialic acid enhances corticospinal axon branching related to target recognition and innervation. J Neurosci 16:5488–5497

80.

Schiff M, Röckle I, Burkhardt H et al (2011) Thalamocortical pathfinding defects precede degeneration of the reticular thalamic nucleus in polysialic acid-deficient mice. J Neurosci 31:1302–1312

81.

Dityatev A, Dityateva G, Schachner M (2000) Synaptic strength as a function of post- versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron 26:207–217

82.

Dityatev A, Dityateva G, Sytnyk V et al (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24:9372–9382

83.

Di Cristo G, Chattopadhyaya B, Kuhlman SJ et al (2007) Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nat Neurosci 10:1569–1577

84.

Hildebrandt H, Becker C, Mürau M et al (1998) Heterogeneous expression of the polysialyltransferases ST8SiaII and ST8SiaIV during postnatal rat brain development. J Neurochem 71:2339–2348

85.

Brennaman LH, Maness PF (2008) Developmental regulation of GABAergic interneuron branching and synaptic development in the prefrontal cortex by soluble neural cell adhesion molecule. Mol Cell Neurosci 37:781–793

86.

Belanger MC, Di Cristo G (2011) Sensory experience differentially modulates the mRNA expression of the polysialyltransferases ST8SiaII and ST8SiaIV in postnatal mouse visual cortex. PLoS One 6:e24874

87.

Cox ET, Brennaman LH, Gable KL et al (2009) Developmental regulation of neural cell adhesion molecule in human prefrontal cortex. Neuroscience 162:96–105

88.

Franceschini I, Angata K, Ong E et al (2001) Polysialyltransferase ST8SiaII (STX) polysialylates all of the major isoforms of NCAM and facilitates neurite outgrowth. Glycobiology 11:231–239

89.

Bhat S, Silberberg DH (1986) Oligodendrocyte cell adhesion molecules are related to neural cell adhesion molecule (N-CAM). J Neurosci 6:3348–3354

90.

Bhat S, Silberberg DH (1988) Developmental expression of neural cell adhesion molecules of oligodendrocytes in vivo and in culture. J Neurochem 50:1830–1838

91.

Trotter J, Bitter-Suermann D, Schachner M (1989) Differentiation-regulated loss of the polysialylated embryonic form and expression of the different polypeptides of the neural cell adhesion molecule by cultured oligodendrocytes and myelin. J Neurosci Res 22:369–383

92.

Nait-Oumesmar B, Vignais L, Duhamel-Clerin E et al (1995) Expression of the highly polysialylated neural cell adhesion molecule during postnatal myelination and following chemically induced demyelination of the adult mouse spinal cord. Eur J Neurosci 7:480–491

93.

Ben-Hur T, Rogister B, Murray K et al (1998) Growth and fate of PSA-NCAM + precursors of the postnatal brain. J Neurosci 18:5777–5788

94.

Nait-Oumesmar B, Decker L, Lachapelle F et al (1999) Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 11:4357–4366

95.

Picard-Riera N, Decker L, Delarasse C et al (2002) Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci USA 99:13211–13216

96.

Nait-Oumesmar B, Picard-Riera N, Kerninon C et al (2007) Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci USA 104:4694–4699

97.

Kornack DR, Rakic P (2001) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA 98:4752–4757

98.

Ponti G, Aimar P, Bonfanti L (2006) Cellular composition and cytoarchitecture of the rabbit subventricular zone and its extensions in the forebrain. J Comp Neurol 498:491–507

99.

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

100.

Seki T, Arai Y (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13:2351–2358

101.

Seki T (2002) Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci Res 70:327–334

102.

Seki T (2002) Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J Neurosci Res 69:772–783

103.

Seri B, Garcia-Verdugo JM, Collado-Morente L et al (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359–378

104.

Seki T, Namba T, Mochizuki H et al (2007) Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502:275–290

105.

Bernier PJ, Vinet J, Cossette M et al (2000) Characterization of the subventricular zone of the adult human brain: evidence for the involvement of Bcl-2. Neurosci Res 37:67–78

106.

Curtis MA, Kam M, Nannmark U et al (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249

107.

Knoth R, Singec I, Ditter M et al (2010) Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One 5:e8809

108.

Varea E, Nacher J, Blasco-Ibanez JM et al (2005) PSA-NCAM expression in the rat medial prefrontal cortex. Neuroscience 136:435–443

109.

Varea E, Castillo-Gomez E, Gomez-Climent MA et al (2007) PSA-NCAM expression in the human prefrontal cortex. J Chem Neuroanat 33:202–209

110.

Nacher J, Alonso-Llosa G, Rosell D et al (2002) PSA-NCAM expression in the piriform cortex of the adult rat. Modulation by NMDA receptor antagonist administration. Brain Res 927:111–121

111.

Nacher J, Blasco-Ibanez JM, McEwen BS (2002) Non-granule PSA-NCAM immunoreactive neurons in the rat hippocampus. Brain Res 930:1–11

112.

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

113.

Gilabert-Juan J, Castillo-Gomez E, Perez-Rando M et al (2011) Chronic stress induces changes in the structure of interneurons and in the expression of molecules related to neuronal structural plasticity and inhibitory neurotransmission in the amygdala of adult mice. Exp Neurol 232:33–40

114.

Gomez-Climent MA, Guirado R, Castillo-Gomez E et al (2011) The polysialylated form of the neural cell adhesion molecule (PSA-NCAM) is expressed in a subpopulation of mature cortical interneurons characterized by reduced structural features and connectivity. Cereb Cortex 21:1028–1041

115.

Gomez-Climent MA, Guirado R, Varea E et al (2010) “Arrested development”. Immature, but not recently generated, neurons in the adult brain. Arch Ital Biol 148:159–172

116.

Nacher J, Crespo C, McEwen BS (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14:629–644

117.

Pekcec A, Loscher W, Potschka H (2006) Neurogenesis in the adult rat piriform cortex. Neuroreport 17:571–574

118.

Gomez-Climent MA, Castillo-Gomez E, Varea E et al (2008) A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood. Cereb Cortex 18:2229–2240

119.

Varea E, Belles M, Vidueira S et al. (2011) PSA-NCAM is expressed in immature, but not recently generated, neurons in the adult cat cerebral cortex layer II. Front Neurosci 5:Article 17. doi:10.3389/fnins.2011.00017

120.

Luzzati F, Bonfanti L, Fasolo A et al (2009) DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cereb Cortex 19:1028–1041

121.

Gomez-Climent MA, Hernandez-Gonzalez S, Shionoya K et al (2011) Olfactory bulbectomy, but not odor conditioned aversion, induces the differentiation of immature neurons in the adult rat piriform cortex. Neuroscience 181:18–27

122.

Bonfanti L, Olive S, Poulain DA et al (1992) 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

123.

Becker CG, Artola A, Gerardy-Schahn R et al (1996) The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. J Neurosci Res 45:143–152

124.

O'Connell AW, Fox GB, Barry T et al (1997) Spatial learning activates neural cell adhesion molecule polysialytion in a corticohippocampal pathway within the medial temporal lobe. J Neurochem 68:2538–2546

125.

Theodosis DT, Poulain DA, Oliet SH (2008) Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 88:983–1008

126.

Theodosis DT, Rougon G, Poulain DA (1991) Retention of embryonic features by an adult neuronal system capable of plasticity: polysialylated neural cell adhesion molecule in the hypothalamo-neurohypophysial system. Proc Natl Acad Sci USA 88:5494–5498

127.

Nothias F, Vernier P, Von Boxberg Y et al (1997) Modulation of NCAM polysialylation is associated with morphofunctional modifications in the hypothalamo-neurohypophysial system during lactation. Eur J Neurosci 9:1553–1565

128.

Theodosis DT, Bonhomme R, Vitiello S et al (1999) Cell surface expression of polysialic acid on NCAM is a prerequisite for activity-dependent morphological neuronal and glial plasticity. J Neurosci 19:10228–10236

129.

Soares S, Von Boxberg Y, Ravaille-Veron M et al (2000) Morphofunctional plasticity in the adult hypothalamus induces regulation of polysialic acid-neural cell adhesion molecule through changing activity and expression levels of polysialyltransferases. J Neurosci 20:2551–2557

130.

Hoyk Z, Parducz A, Theodosis DT (2001) The highly sialylated isoform of the neural cell adhesion molecule is required for estradiol-induced morphological synaptic plasticity in the adult arcuate nucleus. Eur J Neurosci 13:649–656

131.

Monlezun S, Ouali S, Poulain DA et al (2005) Polysialic acid is required for active phases of morphological plasticity of neurosecretory axons and their glia. Mol Cell Neurosci 29:516–524

132.

Kiss JZ, Wang C, Rougon G (1993) Nerve-dependent expression of high polysialic acid neural cell adhesion molecule in neurohypophysial astrocytes of adult rats. Neuroscience 53:213–221

133.

Bolborea M, Laran-Chich MP, Rasri K et al (2011) Melatonin controls photoperiodic changes in tanycyte vimentin and neural cell adhesion molecule expression in the Djungarian hamster (Phodopus sungorus). Endocrinology 152:3871–3883

134.

Le Gal La Salle G, Rougon G, Valin A (1992) The embryonic form of neural cell surface molecule (E-NCAM) in the rat hippocampus and its reexpression on glial cells following kainic acid-induced status epilepticus. J Neurosci 12:872–882

135.

Nomura T, Yabe T, Rosenthal ES et al (2000) PSA-NCAM distinguishes reactive astrocytes in 6-OHDA-lesioned substantia nigra from those in the striatal terminal fields. J Neurosci Res 61:588–596

136.

Camand E, Morel MP, Faissner A et al (2004) Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur J Neurosci 20:1161–1176

137.

Angata K, Nakayama J, Fredette B et al (1997) 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

138.

Kurosawa N, Yoshida Y, Kojima N et al (1997) Polysialic acid synthase (ST8SiaII STX) mRNA expression in the developing mouse central nervous system. J Neurochem 69:494–503

139.

Phillips GR, Krushel LA, Crossin KL (1997) Developmental expression of two rat sialyltransferases that modify the neural cell adhesion molecule, N-CAM. Dev Brain Res 102:143–155

140.

Hildebrandt H, Becker C, Glüer S et al (1998) Polysialic acid on the neural cell adhesion molecule correlates with expression of polysialyltransferases and promotes neuroblastoma cell growth. Cancer Res 58:779–784

141.

Eckhardt M, Bukalo O, Chazal G et al (2000) 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

142.

Nacher J, Guirado R, Varea E et al (2010) Divergent impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid expression in immature neurons and interneurons of the adult cerebral cortex. Neuroscience 167:825–837

143.

Angata K, Long JM, Bukalo O et al (2004) Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J Biol Chem 279:32603–32613

144.

Neale SA, Trasler DG (1994) Early sialylation on N-CAM in splotch neural tube defect mouse embryos. Teratology 50:118–124

145.

Mayanil CS, George D, Mania-Farnell B et al (2000) Overexpression of murine Pax3 increases NCAM polysialylation in a human medulloblastoma cell line. J Biol Chem 275:23259–23266

146.

Mayanil CS, George D, Freilich L et al (2001) Microarray analysis detects novel Pax3 downstream target genes. J Biol Chem 276:49299–49309

147.

Rabinowitz JE, Rutishauser U, Magnuson T (1996) Targeted mutation of Ncam to produce a secreted molecule results in a dominant embryonic lethality. Proc Natl Acad Sci USA 93:6421–6424

148.

Ehlers K, Sturje H, Merker HJ et al (1992) Spina bifida aperta induced by valproic acid and by all-trans-retinoic acid in the mouse: distinct differences in morphology and periods of sensitivity. Teratology 46:117–130

149.

Beecken WD, Engl T, Ogbomo H et al (2005) Valproic acid modulates NCAM polysialylation and polysialyltransferase mRNA expression in human tumor cells. Int Immunopharmacol 5:757–769

150.

Lampen A, Grimaldi PA, Nau H (2005) Modulation of peroxisome proliferator-activated receptor delta activity affects neural cell adhesion molecule and polysialyltransferase ST8SiaIV induction by teratogenic valproic acid analogs in F9 cell differentiation. Mol Pharmacol 68:193–203

151.

Seidenfaden R, Hildebrandt H (2001) Retinoic acid-induced changes in NCAM polysialylation and polysialyltransferase mRNA expression of human neuroblastoma cells. J Neurobiol 46:11–28

152.

Tomasiewicz H, Ono K, Yee D et al (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163–1174

153.

Cremer H, Lange R, Christoph A et al (1994) 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

154.

Weinhold B, Seidenfaden R, Röckle I et al (2005) Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 280:42971–42977

155.

Angata K, Huckaby V, Ranscht B et al (2007) Polysialic acid-directed migration and differentiation of neural precursors is essential for mouse brain development. Mol Cell Biol 27:6659–6668

156.

Durbec P, Cremer H (2001) Revisiting the function of PSA-NCAM in the nervous system. Mol Neurobiol 24:53–64

157.

Hildebrandt H, Mühlenhoff M, Weinhold B et al (2007) Dissecting polysialic acid and NCAM functions in brain development. J Neurochem 103(Suppl 1):56–64

158.

Ono K, Tomasiewicz H, Magnuson T et al (1994) N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13:595–609

159.

Hu H, Tomasiewicz H, Magnuson T et al (1996) The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16:735–743

160.

Chazal G, Durbec P, Jankovski A et al (2000) Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20:1446–1457

161.

Cremer H, Chazal G, Goridis C et al (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323–335

162.

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

163.

Radyushkin K, Anokhin K, Meyer BI et al (2005) Genetic ablation of the mammillary bodies in the Foxb1 mutant mouse leads to selective deficit of spatial working memory. Eur J Neurosci 21:219–229

164.

Rolf B, Bastmeyer M, Schachner M et al (2002) Pathfinding errors of corticospinal axons in neural cell adhesion molecule-deficient mice. J Neurosci 22:8357–8362

165.

Hildebrandt H, Mühlenhoff M, Oltmann-Norden I et al (2009) Imbalance of neural cell adhesion molecule and polysialyltransferase alleles causes defective brain connectivity. Brain 132:2831–2838

166.

Nishiyama A, Komitova M, Suzuki R et al (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10:9–22

167.

Trotter J, Karram K, Nishiyama A (2010) NG2 cells: properties, progeny and origin. Brain Res Rev 63:72–82

168.

Biederer T, Sara Y, Mozhayeva M et al (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525–1531

169.

Kukley M, Capetillo-Zarate E, Dietrich D (2007) Vesicular glutamate release from axons in white matter. Nat Neurosci 10:311–320

170.

Ziskin JL, Nishiyama A, Rubio M et al (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10:321–330

171.

Wang C, Rougon G, Kiss JZ (1994) Requirement of polysialic acid for the migration of the O-2A glial progenitor cell from neurohypophyseal explants. J Neurosci 14:4446–4457

172.

Zhang H, Vutskits L, Calaora V et al (2004) A role for the polysialic acid-neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells. J Cell Sci 117:93–103

173.

Glaser T, Brose C, Franceschini I et al (2007) Neural cell adhesion molecule polysialylation enhances the sensitivity of embryonic stem cell-derived neural precursors to migration guidance cues. Stem Cells 25:3016–3025

174.

Decker L, Avellana-Adalid V, Nait-Oumesmar B et al (2000) Oligodendrocyte precursor migration and differentiation: combined effects of PSA residues, growth factors, and substrates. Mol Cell Neurosci 16:422–439

175.

Decker L, Durbec P, Rougon G et al (2002) Loss of polysialic residues accelerates CNS neural precursor differentiation in pathological conditions. Mol Cell Neurosci 19:225–238

176.

Franceschini I, Vitry S, Padilla F et al (2004) Migrating and myelinating potential of neural precursors engineered to overexpress PSA-NCAM. Mol Cell Neurosci 27:151–162

177.

Charles P, Hernandez MP, Stankoff B et al (2000) Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci USA 97:7585–7590

178.

Fewou SN, Ramakrishnan H, Bussow H et al (2007) Down-regulation of polysialic acid is required for efficient myelin formation. J Biol Chem 282:16700–16711

179.

Doetsch F (2003) A niche for adult neural stem cells. Curr Opin Genet Dev 13:543–550

180.

Kempermann G, Jessberger S, Steiner B et al (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447–452

181.

Petridis AK, El Maarouf A, Rutishauser U (2004) Polysialic acid regulates cell contact-dependent neuronal differentiation of progenitor cells from the subventricular zone. Dev Dyn 230:675–684

182.

Burgess A, Wainwright SR, Shihabuddin LS et al (2008) Polysialic acid regulates the clustering, migration, and neuronal differentiation of progenitor cells in the adult hippocampus. Dev Neurobiol 68:1580–1590

183.

Röckle I, Seidenfaden R, Weinhold B et al (2008) Polysialic acid controls NCAM-induced differentiation of neuronal precursors into calretinin-positive olfactory bulb interneurons. Dev Neurobiol 68:1170–1184

184.

Amoureux MC, Cunningham BA, Edelman GM et al (2000) N-CAM binding inhibits the proliferation of hippocampal progenitor cells and promotes their differentiation to a neuronal phenotype. J Neurosci 20:3631–3640

185.

Kolkova K, Novitskaya V, Pedersen N et al (2000) Neural cell adhesion molecule-stimulated neurite outgrowth depends on activation of protein kinase C and the ras-mitogen-activated protein kinase pathway. J Neurosci 20:2238–2246

186.

Cavallaro U, Niedermeyer J, Fuxa M et al (2001) N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat Cell Biol 3:650–657

187.

Niethammer P, Delling M, Sytnyk V et al (2002) Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 157:521–532

188.

Hinsby AM, Lundfald L, Ditlevsen DK et al (2004) ShcA regulates neurite outgrowth stimulated by neural cell adhesion molecule but not by fibroblast growth factor 2: evidence for a distinct fibroblast growth factor receptor response to neural cell adhesion molecule activation. J Neurochem 91:694–703

189.

Francavilla C, Cattaneo P, Berezin V et al (2009) The binding of NCAM to FGFR1 induces a specific cellular response mediated by receptor trafficking. J Cell Biol 187:1101–1116

190.

Robles E, Gomez TM (2006) Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat Neurosci 9:1274–1283

191.

Muller D, Wang C, Skibo G et al (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17:413–422

192.

Dityatev A (2006) Synaptic functions of the neural cell adhesion molecule (NCAM). In: Dityatev A, El Husseini A (eds) Molecular mechanisms of synaptogenesis. Springer, New York

193.

Vogt J, Glumm R, Schluter L et al (2012) Homeostatic regulation of NCAM polysialylation is critical for correct synaptic targeting. Cell Mol Life Sci 69:1179–1191

194.

Horstkorte R, Mühlenhoff M, Reutter W et al (2004) Selective inhibition of polysialyltransferase ST8SiaII by unnatural sialic acids. Exp Cell Res 298:268–274

195.

Bouzioukh F, Tell F, Jean A et al (2001) NMDA receptor and nitric oxide synthase activation regulate polysialylated neural cell adhesion molecule expression in adult brainstem synapses. J Neurosci 21:4721–4730

196.

Kochlamazashvili G, Senkov O, Grebenyuk S et al (2010) Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors. J Neurosci 30:4171–4183

197.

Kochlamazashvili G, Bukalo O, Senkov O et al (2012) Restoration of synaptic plasticity and learning in young and aged NCAM-deficient mice by enhancing neurotransmission mediated by GluN2A-containing NMDA receptors. J Neurosci 32:2263–2275

198.

Pillai-Nair N, Panicker AK, Rodriguiz RM et al (2005) Neural cell adhesion molecule-secreting transgenic mice display abnormalities in GABAergic interneurons and alterations in behavior. J Neurosci 25:4659–4671

199.

Brennaman LH, Zhang X, Guan H et al (2012) Polysialylated NCAM and EphrinA/EphA regulate synaptic development of GABAergic interneurons in prefrontal cortex. Cereb Cortex. doi:10.1093/cercor/bhr392 (e-pub ahead of print)

200.

Lüthi A, Laurent JP, Figurov A et al (1994) Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372:777–779

201.

Bukalo O, Fentrop N, Lee AY et al (2004) Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus. J Neurosci 24:1565–1577

202.

Cremer H, Chazal G, Carleton A et al (1998) Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc Natl Acad Sci USA 95:13242–13247

203.

Stoenica L, Senkov O, Gerardy-Schahn R et al (2006) In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid. Eur J Neurosci 23:2255–2264

204.

Brennaman LH, Kochlamazashvili G, Stoenica L et al (2011) Transgenic mice overexpressing the extracellular domain of NCAM are impaired in working memory and cortical plasticity. Neurobiol Dis 43:372–378

205.

Staubli U, Chun D, Lynch G (1998) Time-dependent reversal of long-term potentiation by an integrin antagonist. J Neurosci 18:3460–3469

206.

Fux CM, Krug M, Dityatev A et al (2003) NCAM180 and glutamate receptor subtypes in potentiated spine synapses: an immunogold electron microscopic study. Mol Cell Neurosci 24:939–950

207.

Vaithianathan T, Matthias K, Bahr B et al (2004) 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

208.

Senkov O, Sun M, Weinhold B et al (2006) Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J Neurosci 26:10888–10898

209.

Hammond MS, Sims C, Parameshwaran K et al (2006) NCAM associated polysialic acid inhibits NR2B-containing NMDA receptors and prevents glutamate-induced cell death. J Biol Chem 281:34859–34869

210.

Li S, Tian X, Hartley DM et al (2006) Distinct roles for Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-term potentiation and long-term depression. J Neurosci 26:1721–1729

211.

Butler MP, O'Connor JJ, Moynagh PN (2004) Dissection of tumor-necrosis factor-alpha inhibition of long-term potentiation (LTP) reveals a p38 mitogen-activated protein kinase-dependent mechanism which maps to early-but not late-phase LTP. Neuroscience 124:319–326

212.

Empson RM, Buckby LE, Kraus M et al (2006) The cell adhesion molecule neuroplastin-65 inhibits hippocampal long-term potentiation via a mitogen-activated protein kinase p38-dependent reduction in surface expression of GluR1-containing glutamate receptors. J Neurochem 99:850–860

213.

Hsieh H, Boehm J, Sato C et al (2006) AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52:831–843

214.

Bukalo O, Schachner M, Dityatev A (2007) Hippocampal metaplasticity induced by deficiency in the extracellular matrix glycoprotein tenascin-R. J Neurosci 27:6019–6028

215.

Murphy KJ, Oconnell AW, Regan CM (1996) Repetitive and transient increases in hippocampal neural cell adhesion molecule polysialylation state following multitrial spatial training. J Neurochem 67:1268–1274

216.

Ni Dhuill CM, Fox GB, Pittock SJ et al (1999) Polysialylated neural cell adhesion molecule expression in the dentate gyrus of the human hippocampal formation from infancy to old age. J Neurosci Res 55:99–106

217.

Sandi C, Merino JJ, Cordero MI et al (2003) Modulation of hippocampal NCAM polysialylation and spatial memory consolidation by fear conditioning. Biol Psychiatry 54:599–607

218.

Venero C, Herrero AI, Touyarot K et al (2006) Hippocampal up-regulation of NCAM expression and polysialylation plays a key role on spatial memory. Eur J Neurosci 23:1585–1595

219.

Arami S, Jucker M, Schachner M et al (1996) The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav Brain Res 81:81–87

220.

Stork O, Welzl H, Wolfer D et al (2000) Recovery of emotional behaviour in neural cell adhesion molecule (NCAM) null mutant mice through transgenic expression of NCAM180 (in process citation). Eur J Neurosci 12:3291–3306

221.

Bisaz R, Sandi C (2012) Vulnerability of conditional NCAM-deficient mice to develop stress-induced behavioral alterations. Stress 15:195–206

222.

Markram K, Gerardy-Schahn R, Sandi C (2007) Selective learning and memory impairments in mice deficient for polysialylated NCAM in adulthood. Neuroscience 144:788–796

223.

Florian C, Foltz J, Norreel JC et al (2006) Post-training intrahippocampal injection of synthetic poly-alpha-2,8-sialic acid-neural cell adhesion molecule mimetic peptide improves spatial long-term performance in mice. Learn Mem 13:335–341

224.

Mikkonen M, Soininen H, Kalvianen R et al (1998) Remodeling of neuronal circuitries in human temporal lobe epilepsy: increased expression of highly polysialylated neural cell adhesion molecule in the hippocampus and the entorhinal cortex. Ann Neurol 44:923–934

225.

Pekcec A, Mühlenhoff M, Gerardy-Schahn R et al (2007) Impact of the PSA-NCAM system on pathophysiology in a chronic rodent model of temporal lobe epilepsy. Neurobiol Dis 27:54–66

226.

Pekcec A, Fuest C, Mühlenhoff M et al (2008) Targeting epileptogenesis-associated induction of neurogenesis by enzymatic depolysialylation of NCAM counteracts spatial learning dysfunction but fails to impact epilepsy development. J Neurochem 105:389–400

227.

Pekcec A, Weinhold B, Gerardy-Schahn R et al (2010) Polysialic acid affects pathophysiological consequences of status epilepticus. Neuroreport 21:549–553

228.

Garcia-Morales I, de la Pena MP, Kanner AM (2008) Psychiatric comorbidities in epilepsy: identification and treatment. Neurologist 14:S15–S25

229.

Duveau V, Fritschy JM (2010) PSA-NCAM-dependent GDNF signaling limits neurodegeneration and epileptogenesis in temporal lobe epilepsy. Eur J Neurosci 32:89–98

230.

Duveau V, Arthaud S, Rougier A et al (2007) Polysialylation of NCAM is upregulated by hyperthermia and participates in heat shock preconditioning-induced neuroprotection. Neurobiol Dis 26:385–395

231.

Yew DT, Li WP, Webb SE et al (1999) Neurotransmitters, peptides, and neural cell adhesion molecules in the cortices of normal elderly humans and Alzheimer patients: a comparison. Exp Gerontol 34:117–133

232.

Mikkonen M, Soininen H, Tapiola T et al (1999) Hippocampal plasticity in Alzheimer's disease: changes in highly polysialylated NCAM immunoreactivity in the hippocampal formation. Eur J Neurosci 11:1754–1764

233.

Limon ID, Ramirez E, Diaz A et al (2011) Alteration of the sialylation pattern and memory deficits by injection of Abeta (25–35) into the hippocampus of rats. Neurosci Lett 495:11–16

234.

Thomas SN, Soreghan BA, Nistor M et al (2005) Reduced neuronal expression of synaptic transmission modulator HNK-1/neural cell adhesion molecule as a potential consequence of amyloid beta-mediated oxidative stress: a proteomic approach. J Neurochem 92:705–717

235.

Mehanna A, Jakovcevski I, Acar A et al (2010) Polysialic acid glycomimetic promotes functional recovery and plasticity after spinal cord injury in mice. Mol Ther 18:34–43

236.

Berezin V, Bock E (2010) NCAM mimetic peptides: an update. Adv Exp Med Biol 663:337–353

237.

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

238.

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

239.

Wang Y, Neumann H (2010) Alleviation of neurotoxicity by microglial human Siglec-11. J Neurosci 30:3482–3488

240.

Charles P, Reynolds R, Seilhean D et al (2002) Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis? Brain 125:1972–1979

241.

Takikita S, Fukuda T, Mohri I et al (2004) Perturbed myelination process of premyelinating oligodendrocyte in Niemann–Pick type C mouse. J Neuropathol Exp Neurol 63:660–673

242.

Koutsoudaki PN, Hildebrandt H, Gudi V et al (2010) Remyelination after cuprizone induced demyelination is accelerated in mice deficient in the polysialic acid synthesizing enzyme St8siaIV. Neuroscience 171:235–244

243.

Koutsoudaki PN, Skripuletz T, Gudi V et al (2009) Demyelination of the hippocampus is prominent in the cuprizone model. Neurosci Lett 451:83–88

244.

Skripuletz T, Gudi V, Hackstette D et al (2011) De- and remyelination in the CNS white and grey matter induced by cuprizone: the old, the new, and the unexpected. Histol Histopathol 26:1585–1597

245.

Vawter MP (2000) Dysregulation of the neural cell adhesion molecule and neuropsychiatric disorders. Eur J Pharmacol 405:385–395

246.

Brennaman LH, Maness PF (2010) NCAM in neuropsychiatric and neurodegenerative disorders. Adv Exp Med Biol 663:299–317

247.

Plioplys AV, Hemmens SE, Regan CM (1990) Expression of a neural cell adhesion molecule serum fragment is depressed in autism. J Neuropsychiatry Clin Neurosci 2:413–417

248.

Purcell AE, Rocco MM, Lenhart JA et al (2001) Assessment of neural cell adhesion molecule (NCAM) in autistic serum and postmortem brain. J Autism Dev Disord 31:183–194

249.

Barbeau D, Liang JJ, Robitalille Y et al (1995) Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc Natl Acad Sci USA 92:2785–2789

250.

Varea E, Guirado R, Gilabert-Juan J et al (2012) Expression of PSA-NCAM and synaptic proteins in the amygdala of psychiatric disorder patients. J Psychiatr Res 46:189–197

251.

Purcell SM, Wray NR, Stone JL et al (2009) Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 460:748–752

252.

Stefansson H, Ophoff RA, Steinberg S et al (2009) Common variants conferring risk of schizophrenia. Nature 460:744–747

253.

Lewis CM, Levinson DF, Wise LH et al (2003) Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: schizophrenia. Am J Hum Genet 73:34–48

254.

Lindholm E, Aberg K, Ekholm B et al (2004) Reconstruction of ancestral haplotypes in a 12-generation schizophrenia pedigree. Psychiatr Genet 14:1–8

255.

Maziade M, Roy MA, Chagnon YC et al (2005) Shared and specific susceptibility loci for schizophrenia and bipolar disorder: a dense genome scan in Eastern Quebec families. Mol Psychiatry 10:486–499

256.

Arai M, Yamada K, Toyota T et al (2006) Association between polymorphisms in the promoter region of the sialyltransferase 8B (SIAT8B) gene and schizophrenia. Biol Psychiatry 59:652–659

257.

Atz ME, Rollins B, Vawter MP (2007) NCAM1 association study of bipolar disorder and schizophrenia: polymorphisms and alternatively spliced isoforms lead to similarities and differences. Psychiatr Genet 17:55–67

258.

Sullivan PF, Keefe RS, Lange LA et al (2007) NCAM1 and neurocognition in schizophrenia. Biol Psychiatry 61:902–910

259.

Tao R, Li C, Zheng Y et al (2007) Positive association between SIAT8B and schizophrenia in the Chinese Han population. Schizophr Res 90:108–114

260.

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

261.

Arai M, Itokawa M, Yamada K et al (2004) Association of neural cell adhesion molecule 1 gene polymorphisms with bipolar affective disorder in Japanese individuals. Biol Psychiatry 55:804–810

262.

Lee MT, Chen CH, Lee CS et al (2011) Genome-wide association study of bipolar I disorder in the Han Chinese population. Mol Psychiatry 16:548–556

263.

Vazza G, Bertolin C, Scudellaro E et al (2007) Genome-wide scan supports the existence of a susceptibility locus for schizophrenia and bipolar disorder on chromosome 15q26. Mol Psychiatry 12:87–93

264.

Anney R, Klei L, Pinto D et al (2010) A genome-wide scan for common alleles affecting risk for autism. Hum Mol Genet 19:4072–4082

265.

Lewis DA, Levitt P (2002) Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25:409–432

266.

Begre S, Koenig T (2008) Cerebral disconnectivity: an early event in schizophrenia. Neuroscientist 14:19–45

267.

Shenton ME, Dickey CC, Frumin M et al (2001) A review of MRI findings in schizophrenia. Schizophr Res 49:1–52

268.

Wood GK, Tomasiewicz H, Rutishauser U et al (1998) NCAM-180 knockout mice display increased lateral ventricle size and reduced prepulse inhibition of startle. Neuroreport 9:461–466

269.

Turetsky BI, Moberg PJ, Yousem DM et al (2000) Reduced olfactory bulb volume in patients with schizophrenia. Am J Psychiatry 157:828–830

270.

Innocenti GM, Ansermet F, Parnas J (2003) Schizophrenia, neurodevelopment and corpus callosum. Mol Psychiatry 8:261–274

271.

Hulshoff Pol HE, Schnack HG, Mandl RC et al (2004) Focal white matter density changes in schizophrenia: reduced inter-hemispheric connectivity. Neuroimage 21:27–35

272.

Douaud G, Smith S, Jenkinson M et al (2007) Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain 130:2375–2386

273.

Mitelman SA, Torosjan Y, Newmark RE et al (2007) Internal capsule, corpus callosum and long associative fibers in good and poor outcome schizophrenia: a diffusion tensor imaging survey. Schizophr Res 92:211–224

274.

Barch DM (2005) The cognitive neuroscience of schizophrenia. Annu Rev Clin Psychol 1:321–353

275.

Plappert CF, Schachner M, Pilz PK (2005) Neural cell adhesion molecule-null mice are not deficient in prepulse inhibition of the startle response. Neuroreport 16:1009–1012

276.

Sandi C, Merino JJ, Cordero MI et al (2001) Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience 102:329–339

277.

Pham K, Nacher J, Hof PR et al (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17:879–886

278.

Uchida S, Hara K, Kobayashi A et al (2011) Impaired hippocampal spinogenesis and neurogenesis and altered affective behavior in mice lacking heat shock factor 1. Proc Natl Acad Sci USA 108:1681–1686

279.

Nacher J, Pham K, Gil-Fernandez V et al (2004) Chronic restraint stress and chronic corticosterone treatment modulate differentially the expression of molecules related to structural plasticity in the adult rat piriform cortex. Neuroscience 126:503–509

280.

Cordero MI, Rodriguez JJ, Davies HA et al (2005) Chronic restraint stress down-regulates amygdaloid expression of polysialylated neural cell adhesion molecule. Neuroscience 133:903–910

281.

Gilabert-Juan J, Molto MD, Nacher J (2012) Post-weaning social isolation rearing influences the expression of molecules related to inhibitory neurotransmission and structural plasticity in the amygdala of adult rats. Brain Res 1448:129–136. doi:10.1016/j.brainres.2012.01.073

282.

Lewis DA, Sweet RA (2009) Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. J Clin Invest 119:706–716

283.

Castren E (2005) Is mood chemistry? Nat Rev Neurosci 6:241–246

284.

McEwen BS, Eiland L, Hunter RG et al (2012) Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62:3–12

285.

Varea E, Blasco-Ibanez JM, Gomez-Climent MA et al (2007) Chronic fluoxetine treatment increases the expression of PSA-NCAM in the medial prefrontal cortex. Neuropsychopharmacology 32:803–812

286.

Varea E, Castillo-Gomez E, Gomez-Climent MA et al (2007) Chronic antidepressant treatment induces contrasting patterns of synaptophysin and PSA-NCAM expression in different regions of the adult rat telencephalon. Eur Neuropsychopharmacol 17:546–557

287.

Guirado R, Sanchez-Matarredona D, Varea E et al (2012) Chronic fluoxetine treatment in middle-aged rats induces changes in the expression of plasticity-related molecules and in neurogenesis. BMC Neurosci 13:5

288.

Guirado R, Varea E, Castillo-Gomez E et al (2009) Effects of chronic fluoxetine treatment on the rat somatosensory cortex: activation and induction of neuronal structural plasticity. Neurosci Lett 457:12–15

289.

Sairanen M, O'Leary OF, Knuuttila JE et al (2007) Chronic antidepressant treatment selectively increases expression of plasticity-related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience 144:368–374

290.

Castillo-Gomez E, Gomez-Climent MA, Varea E et al (2008) Dopamine acting through D2 receptors modulates the expression of PSA-NCAM, a molecule related to neuronal structural plasticity, in the medial prefrontal cortex of adult rats. Exp Neurol 214:97–111

291.

Castillo-Gomez E, Varea E, Blasco-Ibanez JM et al (2011) Polysialic acid is required for dopamine D2 receptor-mediated plasticity involving inhibitory circuits of the rat medial prefrontal cortex. PLoS One 6:e29516

Title: Polysialic Acid in Brain Development and Synaptic Plasticity
Authors: Herbert Hildebrandt
Alexander Dityatev
Publisher: Springer Berlin Heidelberg
Book: SialoGlyco Chemistry and Biology I
Print ISBN: 978-3-662-47939-1

Electronic ISBN: 978-3-662-47940-7

Copyright Year: 2015
DOI: https://doi.org/10.1007/128_2013_446