Skip to main content

Glycolipid and Glycoprotein Expression During Neural Development

  • Chapter
  • First Online:

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 9))

Abstract

In mammals, the central and peripheral nervous systems are developmentally derived from cells in the neural plate. Specific ectodermal cells in this area form the neural tube and neural crest during the early developmental stage. The neural tube is the origin of the central nervous system which consists of both the brain and spinal cord, whereas neural crest cells are precursors of the peripheral nervous system. During neural tube formation and neural crest development, carbohydrate-rich molecules, including glycolipids, glycoproteins, and proteoglycans, are expressed primarily on the outer surface of cell plasma membranes. The structural diversity of their carbohydrate moieties coupled with their expression at different stages of development makes these molecules excellent biomarkers for various cell types. In addition, these molecules play crucial functional roles in cell proliferation, differentiation, interaction, migration, and signal transduction. In this chapter, we discuss the expression profiles and potential functional roles of glycoconjugates during neural development.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

BLBP:

Brain lipid-binding protein

BMB:

Bone morphogenetic protein

CD:

Cluster of differentiation

Cer:

Ceramide

CNS:

Central nervous system

CNTF:

Ciliary neurotrophic factor

CS:

Chondroitin sulfate

CSPG:

Chondroitin sulfate proteoglycan

CST:

Cerebroside sulfotransferase

Dll1:

Delta-like1

EGF:

Epidermal growth factor

FABP7:

Fatty acid-binding protein 7

FGF:

Fibroblast growth factor

Fuc:

Fucose

FUT:

Fucosyltransferase

GAG:

Glycosaminoglycan

GalCer:

Galactosylceramide

GalNAcT:

N-acetylgalactosaminyltransferase

GalT:

Galactosyltransferase

GFAP:

Glial fibrillary acidic protein

GlcAT-P:

UDP-glucuronyltransferase-P

GlcCer:

Glucosylceramide

GlcT:

Glucosyltransferase

GRP:

Glial-restricted precursor

GSL:

Glycosphingolipid

HA:

Hyaluronic acid

HNK-1:

Human natural killer-1 antigen

HS:

Heparin sulfate

HSPG:

Heparin sulfate proteoglycan

IL-6:

Interleukin 6

INP:

Intermediate neuronal progenitor cell

IPC:

Intermediate progenitor cell

JAK-STAT:

Janus kinase (JAK)-signal transducer and activator of transcription 3 (STAT3)

LacCer:

Lactosylceramide

Lfng :

Lunatic fringe

MA:

Cerebral mantle

mAb:

Monoclonal antibody

MAPK:

Mitogen-activated protein kinase

MZ:

Marginal zone

NEC:

Neuroepithelial cell

NG-2:

Nerve/glial antigen 2

NRP:

Neuronal restricted progenitor

NSC:

Neural stem cell

OPC:

Oligodendrocyte precursor cell

PDGF:

Platelet-derived growth factor

PG:

Proteoglycan

PHA-E4:

Phaseolus vulgaris erythroagglutinating lectin

PNA:

Peanut agglutinin

PNS:

Peripheral nervous system

PSA-NCAM:

Polysialic acid-neural cell adhesion molecule

PST:

ST8SiaIV

RGC:

Radial glial cell

SGZ:

Subgranular zone

SSEA:

Stage-specific embryonic antigen

ST:

Sialyltransferase

STX:

ST8SiaII

SVZ:

Subventricular zone

VZ:

Ventricular zone

References

  • IUPAC-IUB Commission on Biochemical Nomenclature. The nomenclature of lipids. Recommendations (1976) Lipids. 1977;12(6):455–68.

    Google Scholar 

  • Aaku-Saraste E, Hellwig A, Huttner WB. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-remodeling of the neuroepithelium prior to neurogenesis. Dev Biol. 1996;180(2):664–79.

    CAS  PubMed  Google Scholar 

  • Abo T, Balch CM. A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol. 1981;127(3):1024–9.

    CAS  PubMed  Google Scholar 

  • Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G, et al. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol. 2007;25(7):803–16.

    CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci. 2001;2(4):287–93.

    CAS  PubMed  Google Scholar 

  • Anderson DJ. Cellular and molecular biology of neural crest cell lineage determination. Trends Genet. 1997;13(7):276–80.

    CAS  PubMed  Google Scholar 

  • Ando S, Yu RK. Isolation and characterization of two isomers of brain tetrasialogangliosides. J Biol Chem. 1979;254(23):12224–9.

    CAS  PubMed  Google Scholar 

  • Angata K, Fukuda M. Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie. 2003;85(1–2):195–206.

    CAS  PubMed  Google Scholar 

  • Angata K, Long JM, Bukalo O, Lee W, Dityatev A, Wynshaw-Boris A, et al. Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J Biol Chem. 2004;279(31):32603–13.

    CAS  PubMed  Google Scholar 

  • Ariga T, Kohriyama T, Freddo L, Latov N, Saito M, Kon K, et al. Characterization of sulfated glucuronic acid containing glycolipids reacting with IgM M-proteins in patients with neuropathy. J Biol Chem. 1987;262(2):848–53.

    CAS  PubMed  Google Scholar 

  • Asou H, Hirano S, Uyemura K. Ganglioside composition of astrocytes. Cell Struct Funct. 1989;14(5):561–8.

    CAS  PubMed  Google Scholar 

  • Attardo A, Calegari F, Haubensak W, Wilsch-Brauninger M, Huttner WB. Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS One. 2008;3(6):e2388.

    PubMed Central  PubMed  Google Scholar 

  • Aubert I, Ridet JL, Gage FH. Regeneration in the adult mammalian CNS: guided by development. Curr Opin Neurobiol. 1995;5(5):625–35.

    CAS  PubMed  Google Scholar 

  • Bannerman PG, Oliver TM, Xu Z, Shieh A, Pleasure DE. Effects of FGF-1 and FGF-2 on GD3 immunoreactive spinal neuroepithelial cells. J Neurosci Res. 1996;45(5):549–57.

    CAS  PubMed  Google Scholar 

  • Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, et al. Galectins: a family of animal beta-galactoside-binding lectins. Cell. 1994;76(4):597–8.

    CAS  PubMed  Google Scholar 

  • Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, et al. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell. 2010;7(6):744–58.

    CAS  PubMed  Google Scholar 

  • Bieberich E, MacKinnon S, Silva J, Yu RK. Regulation of apoptosis during neuronal differentiation by ceramide and b-series complex gangliosides. J Biol Chem. 2001;276(48):44396–404.

    CAS  PubMed  Google Scholar 

  • Bixby S, Kruger GM, Mosher JT, Joseph NM, Morrison SJ. Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron. 2002;35(4):643–56.

    CAS  PubMed  Google Scholar 

  • Blum AS, Barnstable CJ. O-acetylation of a cell-surface carbohydrate creates discrete molecular patterns during neural development. Proc Natl Acad Sci U S A. 1987;84(23):8716–20.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boisseau S, Nedelec J, Poirier V, Rougon G, Simonneau M. Analysis of high PSA N-CAM expression during mammalian spinal cord and peripheral nervous system development. Development. 1991;112(1):69–82.

    CAS  PubMed  Google Scholar 

  • Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, et al. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science. 1997;278(5337):477–83.

    CAS  PubMed  Google Scholar 

  • Bosio A, Binczek E, Stoffel W. Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc Natl Acad Sci U S A. 1996;93(23):13280–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bronner-Fraser M. Perturbation of cranial neural crest migration by the HNK-1 antibody. Dev Biol. 1987;123(2):321–31.

    CAS  PubMed  Google Scholar 

  • Bronner-Fraser M, Fraser SE. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature. 1988;335(6186):161–4.

    CAS  PubMed  Google Scholar 

  • Bruckner G, Biesold D. Histochemistry of glycogen deposition in perinatal rat brain: importance of radial glial cells. J Neurocytol. 1981;10(5):749–57.

    CAS  PubMed  Google Scholar 

  • Bruckner K, Perez L, Clausen H, Cohen S. Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature. 2000;406(6794):411–5.

    CAS  PubMed  Google Scholar 

  • Cammer W, Zhang H. Carbonic anhydrase II in microglia in forebrains of neonatal rats. J Neuroimmunol. 1996a;67(2):131–6.

    CAS  PubMed  Google Scholar 

  • Cammer W, Zhang H. Ganglioside GD3 in radial glia and astrocytes in situ in brains of young and adult mice. J Neurosci Res. 1996b;46(1):18–23.

    CAS  PubMed  Google Scholar 

  • Capela A, Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron. 2002;35(5):865–75.

    PubMed  Google Scholar 

  • Capela A, Temple S. LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev Biol. 2006;291(2):300–13.

    CAS  PubMed  Google Scholar 

  • Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, et al. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci. 2009;12(3):259–67.

    CAS  PubMed  Google Scholar 

  • Chang MY, Park CH, Son H, Lee YS, Lee SH. Developmental stage-dependent self-regulation of embryonic cortical precursor cell survival and differentiation by leukemia inhibitory factor. Cell Death Differ. 2004;11(9):985–96.

    CAS  PubMed  Google Scholar 

  • Charles P, Hernandez MP, Stankoff B, Aigrot MS, Colin C, Rougon G, et al. Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci U S A. 2000;97(13):7585–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci. 1999;19(11):4462–71.

    CAS  PubMed  Google Scholar 

  • Chou DK, Ilyas AA, Evans JE, Costello C, Quarles RH, Jungalwala FB. Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy. J Biol Chem. 1986;261(25):11717–25.

    CAS  PubMed  Google Scholar 

  • Coetzee T, Fujita N, Dupree J, Shi R, Blight A, Suzuki K, et al. Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell. 1996;86(2):209–19.

    CAS  PubMed  Google Scholar 

  • Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci U S A. 2008;105(3):1026–31.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dawson MR, Polito A, Levine JM, Reynolds R. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci. 2003;24(2):476–88.

    CAS  PubMed  Google Scholar 

  • de la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, et al. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development. 1997;124(6):1139–48.

    PubMed  Google Scholar 

  • Derouet D, Rousseau F, Alfonsi F, Froger J, Hermann J, Barbier F, et al. Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. Proc Natl Acad Sci U S A. 2004;101(14):4827–32.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97(6):703–16.

    CAS  PubMed  Google Scholar 

  • Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997;17(13):5046–61.

    CAS  PubMed  Google Scholar 

  • Domowicz M, Li H, Hennig A, Henry J, Vertel BM, Schwartz NB. The biochemically and immunologically distinct CSPG of notochord is a product of the aggrecan gene. Dev Biol. 1995;171(2):655–64.

    CAS  PubMed  Google Scholar 

  • Dong Z, Sinanan A, Parkinson D, Parmantier E, Mirsky R, Jessen KR. Schwann cell development in embryonic mouse nerves. J Neurosci Res. 1999;56(4):334–48.

    CAS  PubMed  Google Scholar 

  • Durbec P, Cremer H. Revisiting the function of PSA-NCAM in the nervous system. Mol Neurobiol. 2001 Aug-Dec;24(1-3):53–64.

    Google Scholar 

  • Dvorak P, Hampl A, Jirmanova L, Pacholikova J, Kusakabe M. Embryoglycan ectodomains regulate biological activity of FGF-2 to embryonic stem cells. J Cell Sci. 1998;111(Pt 19):2945–52.

    CAS  PubMed  Google Scholar 

  • Eckhardt M, Bukalo O, Chazal G, Wang L, Goridis C, Schachner M, et al. 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. 2000;20(14):5234–44.

    CAS  PubMed  Google Scholar 

  • Eisenbarth GS, Walsh FS, Nirenberg M. Monoclonal antibody to a plasma membrane antigen of neurons. Proc Natl Acad Sci U S A. 1979;76(10):4913–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Encinas JM, Vaahtokari A, Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A. 2006;103(21):8233–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Epstein ML, Poulsen KT, Thiboldeaux R. Formation of ganglia in the gut of the chick embryo. J Comp Neurol. 1991;307(2):189–99.

    CAS  PubMed  Google Scholar 

  • Fang Y, Wu G, Xie X, Lu ZH, Ledeen RW. Endogenous GM1 ganglioside of the plasma membrane promotes neuritogenesis by two mechanisms. Neurochem Res. 2000;25(7):931–40.

    CAS  PubMed  Google Scholar 

  • Faure C, Chalazonitis A, Rheaume C, Bouchard G, Sampathkumar SG, Yarema KJ, et al. Gangliogenesis in the enteric nervous system: roles of the polysialylation of the neural cell adhesion molecule and its regulation by bone morphogenetic protein-4. Dev Dyn. 2007;236(1):44–59.

    CAS  PubMed  Google Scholar 

  • Fenderson BA, Eddy EM, Hakomori S. Glycoconjugate expression during embryogenesis and its biological significance. Bioessays. 1990;12(4):173–9.

    CAS  PubMed  Google Scholar 

  • Fenderson BA, Zehavi U, Hakomori S. A multivalent lacto-N-fucopentaose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligosaccharide is ineffective. J Exp Med. 1984;160(5):1591–6.

    CAS  PubMed  Google Scholar 

  • Ffrench-Constant C, Raff MC. The oligodendrocyte-type-2 astrocyte cell lineage is specialized for myelination. Nature. 1986a;323(6086):335–8.

    CAS  PubMed  Google Scholar 

  • Ffrench-Constant C, Raff MC. Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature. 1986b;319(6053):499–502.

    CAS  PubMed  Google Scholar 

  • Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, et al. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci. 2003;23(3):373–82.

    CAS  PubMed  Google Scholar 

  • Finne J, Finne U, Deagostini-Bazin H, Goridis C. Occurrence of alpha 2-8 linked polysialosyl units in a neural cell adhesion molecule. Biochem Biophys Res Commun. 1983;112(2):482–7.

    CAS  PubMed  Google Scholar 

  • Fishell G, Kriegstein A. Cortical development: new concepts. Neuron. 2005;46(3):361–2.

    CAS  PubMed  Google Scholar 

  • Fishell G, Kriegstein AR. Neurons from radial glia: the consequences of asymmetric inheritance. Curr Opin Neurobiol. 2003;13(1):34–41.

    CAS  PubMed  Google Scholar 

  • Franceschini I, Vitry S, Padilla F, Casanova P, Tham TN, Fukuda M, et al. Migrating and myelinating potential of neural precursors engineered to overexpress PSA-NCAM. Mol Cell Neurosci. 2004;27(2):151–62.

    CAS  PubMed  Google Scholar 

  • Franco SJ, Muller U. Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron. 2013;77(1):19–34.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Freischutz B, Saito M, Rahmann H, Yu RK. Activities of five different sialyltransferases in fish and rat brains. J Neurochem. 1994;62(5):1965–73.

    CAS  PubMed  Google Scholar 

  • Freischutz B, Saito M, Rahmann H, Yu RK. Characterization of sialyltransferase-IV activity and its involvement in the c-pathway of brain ganglioside metabolism. J Neurochem. 1995;64(1):385–93.

    CAS  PubMed  Google Scholar 

  • Fu M, Vohra BP, Wind D, Heuckeroth RO. BMP signaling regulates murine enteric nervous system precursor migration, neurite fasciculation, and patterning via altered Ncam1 polysialic acid addition. Dev Biol. 2006;299(1):137–50.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fujita S. The discovery of the matrix cell, the identification of the multipotent neural stem cell and the development of the central nervous system. Cell Struct Funct. 2003;28(4):205–28.

    PubMed  Google Scholar 

  • Fukuda S, Taga T. Cell fate determination regulated by a transcriptional signal network in the developing mouse brain. Anat Sci Int. 2005;80(1):12–8.

    CAS  PubMed  Google Scholar 

  • Furukawa K, Aixinjueluo W, Kasama T, Ohkawa Y, Yoshihara M, Ohmi Y, et al. Disruption of GM2/GD2 synthase gene resulted in overt expression of 9-O-acetyl GD3 irrespective of Tis21. J Neurochem. 2008;105(3):1057–66.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gabay L, Lowell S, Rubin LL, Anderson DJ. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron. 2003;40(3):485–99.

    CAS  PubMed  Google Scholar 

  • Gaiano N, Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci. 2002;25:471–90.

    CAS  PubMed  Google Scholar 

  • Goldman JE, Hirano M, Yu RK, Seyfried TN. GD3 ganglioside is a glycolipid characteristic of immature neuroectodermal cells. J Neuroimmunol. 1984;7(2–3):179–92.

    CAS  PubMed  Google Scholar 

  • Goretzki L, Burg MA, Grako KA, Stallcup WB. High-affinity binding of basic fibroblast growth factor and platelet-derived growth factor-AA to the core protein of the NG2 proteoglycan. J Biol Chem. 1999;274(24):16831–7.

    CAS  PubMed  Google Scholar 

  • Gotz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol. 2005;6(10):777–88.

    PubMed  Google Scholar 

  • Grako KA, Ochiya T, Barritt D, Nishiyama A, Stallcup WB. PDGF (alpha)-receptor is unresponsive to PDGF-AA in aortic smooth muscle cells from the NG2 knockout mouse. J Cell Sci. 1999;112(Pt 6):905–15.

    CAS  PubMed  Google Scholar 

  • Graus-Porta D, Blaess S, Senften M, Littlewood-Evans A, Damsky C, Huang Z, et al. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron. 2001;31(3):367–79.

    CAS  PubMed  Google Scholar 

  • Guan F, Handa K, Hakomori SI. Specific glycosphingolipids mediate epithelial-to-mesenchymal transition of human and mouse epithelial cell lines. Proc Natl Acad Sci U S A. 2009;106(18):7461–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haines N, Irvine KD. Glycosylation regulates Notch signalling. Nat Rev Mol Cell Biol. 2003;4(10):786–97.

    CAS  PubMed  Google Scholar 

  • Hajos F, Woodhams PL, Basco E, Csillag A, Balazs R. Proliferation of astroglia in the embryonic mouse forebrain as revealed by simultaneous immunocytochemistry and autoradiography. Acta Morphol Acad Sci Hung. 1981;29(4):361–4.

    CAS  PubMed  Google Scholar 

  • Hamanoue M, Matsuzaki Y, Sato K, Okano HJ, Shibata S, Sato I, et al. Cell surface N-glycans mediated isolation of mouse neural stem cells. J Neurochem. 2009;110(5):1575–84.

    CAS  PubMed  Google Scholar 

  • Hanjan SN, Kearney JF, Cooper MD. A monoclonal antibody (MMA) that identifies a differentiation antigen on human myelomonocytic cells. Clin Immunol Immunopathol. 1982;23(2):172–88.

    CAS  PubMed  Google Scholar 

  • Hartfuss E, Galli R, Heins N, Gotz M. Characterization of CNS precursor subtypes and radial glia. Dev Biol. 2001;229(1):15–30.

    CAS  PubMed  Google Scholar 

  • Hennen E, Czopka T, Faissner A. Structurally distinct LewisX glycans distinguish subpopulations of neural stem/progenitor cells. J Biol Chem. 2011;286(18):16321–31.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heuckeroth RO, Lampe PA, Johnson EM, Milbrandt J. Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev Biol. 1998;200(1):116–29.

    CAS  PubMed  Google Scholar 

  • Hirahara Y, Bansal R, Honke K, Ikenaka K, Wada Y. Sulfatide is a negative regulator of oligodendrocyte differentiation: development in sulfatide-null mice. Glia. 2004;45(3):269–77.

    PubMed  Google Scholar 

  • Hirschberg K, Zisling R, van Echten-Deckert G, Futerman AH. Ganglioside synthesis during the development of neuronal polarity. Major changes occur during axonogenesis and axon elongation, but not during dendrite growth or synaptogenesis. J Biol Chem. 1996;271(25):14876–82.

    CAS  PubMed  Google Scholar 

  • Holley JA, Yu RK. Localization of glycoconjugates recognized by the HNK-1 antibody in mouse and chick embryos during early neural development. Dev Neurosci. 1987;9(2):105–19.

    CAS  PubMed  Google Scholar 

  • Honke K, Hirahara Y, Dupree J, Suzuki K, Popko B, Fukushima K, et al. Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc Natl Acad Sci U S A. 2002;99(7):4227–32.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hori K, Sen A, Artavanis-Tsakonas S. Notch signaling at a glance. J Cell Sci. 2013;126(Pt 10):2135–40.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hou X, Tashima Y, Stanley P. Galactose differentially modulates lunatic and manic fringe effects on Delta1-induced NOTCH signaling. J Biol Chem. 2012;287(1):474–83.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huttner WB, Zimmerberg J. Implications of lipid microdomains for membrane curvature, budding and fission. Curr Opin Cell Biol. 2001;13(4):478–84.

    CAS  PubMed  Google Scholar 

  • Ichikawa M, Shiga T, Hirata Y. Spatial and temporal pattern of postnatal proliferation of glial cells in the parietal cortex of the rat. Brain Res. 1983;285(2):181–7.

    CAS  PubMed  Google Scholar 

  • Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, et al. The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol. 2001;21(12):3888–900.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ishii Y, Nakamura S, Osumi N. Demarcation of early mammalian cortical development by differential expression of fringe genes. Brain Res Dev Brain Res. 2000;119(2):307–20.

    CAS  PubMed  Google Scholar 

  • Izumikawa T, Kanagawa N, Watamoto Y, Okada M, Saeki M, Sakano M, et al. Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficient mice. J Biol Chem. 2010;285(16):12190–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Janich P, Corbeil D. GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett. 2007;581(9):1783–7.

    CAS  PubMed  Google Scholar 

  • Jirmanova L, Pacholikova J, Krejci P, Hampl A, Dvorak P. O-linked carbohydrates are required for FGF-2-mediated proliferation of mouse embryonic cells. Int J Dev Biol. 1999;43(6):555–62.

    CAS  PubMed  Google Scholar 

  • Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell. 1999;96(1):25–34.

    CAS  PubMed  Google Scholar 

  • Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci. 2002;22(7):2792–803.

    CAS  PubMed  Google Scholar 

  • Jungalwala FB. Expression and biological functions of sulfoglucuronyl glycolipids (SGGLs) in the nervous system – a review. Neurochem Res. 1994;19(8):945–57.

    CAS  PubMed  Google Scholar 

  • Kabos P, Matundan H, Zandian M, Bertolotto C, Robinson ML, Davy BE, et al. Neural precursors express multiple chondroitin sulfate proteoglycans, including the lectican family. Biochem Biophys Res Commun. 2004;318(4):955–63.

    CAS  PubMed  Google Scholar 

  • Kamakura S, Oishi K, Yoshimatsu T, Nakafuku M, Masuyama N, Gotoh Y. Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol. 2004;6(6):547–54.

    CAS  PubMed  Google Scholar 

  • Kasai N, Yu RK. The monoclonal antibody A2B5 is specific to ganglioside GQ1c. Brain Res. 1983;277(1):155–8.

    CAS  PubMed  Google Scholar 

  • Kato TM, Kawaguchi A, Kosodo Y, Niwa H, Matsuzaki F. Lunatic fringe potentiates Notch signaling in the developing brain. Mol Cell Neurosci. 2010;45(1):12–25.

    CAS  PubMed  Google Scholar 

  • Kawai H, Allende ML, Wada R, Kono M, Sango K, Deng C, et al. Mice expressing only monosialoganglioside GM3 exhibit lethal audiogenic seizures. J Biol Chem. 2001;276(10):6885–8.

    CAS  PubMed  Google Scholar 

  • Kinoshita MO, Furuya S, Ito S, Shinoda Y, Yamazaki Y, Greimel P, et al. Lipid rafts enriched in phosphatidylglucoside direct astroglial differentiation by regulating tyrosine kinase activity of epidermal growth factor receptors. Biochem J. 2009a;419(3):565–75.

    CAS  PubMed  Google Scholar 

  • Kinoshita MO, Shinoda Y, Sakai K, Hashikawa T, Watanabe M, Machida T, et al. Selective upregulation of 3-phosphoglycerate dehydrogenase (Phgdh) expression in adult subventricular zone neurogenic niche. Neurosci Lett. 2009b;453(1):21–6.

    CAS  PubMed  Google Scholar 

  • Kitada M, Kuroda Y, Dezawa M. Lectins as a tool for detecting neural stem/progenitor cells in the adult mouse brain. Anat Rec (Hoboken). 2011;294(2):305–21.

    Google Scholar 

  • Kleene R, Schachner M. Glycans and neural cell interactions. Nat Rev Neurosci. 2004;5(3):195–208.

    CAS  PubMed  Google Scholar 

  • Koch U, Lehal R, Radtke F. Stem cells living with a Notch. Development. 2013;140(4):689–704.

    CAS  PubMed  Google Scholar 

  • Kondo T, Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science. 2000;289(5485):1754–7.

    CAS  PubMed  Google Scholar 

  • Kondo T, Raff M. Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells. Genes Dev. 2004;18(23):2963–72.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci. 2009;32:149–84.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kruse J, Mailhammer R, Wernecke H, Faissner A, Sommer I, Goridis C, et al. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature. 1984;311(5982):153–5.

    CAS  PubMed  Google Scholar 

  • Kudo T, Fujii T, Ikegami S, Inokuchi K, Takayama Y, Ikehara Y, et al. Mice lacking alpha1,3-fucosyltransferase IX demonstrate disappearance of Lewis x structure in brain and increased anxiety-like behaviors. Glycobiology. 2007;17(1):1–9.

    CAS  PubMed  Google Scholar 

  • Kudo T, Ikehara Y, Togayachi A, Kaneko M, Hiraga T, Sasaki K, et al. Expression cloning and characterization of a novel murine alpha1, 3-fucosyltransferase, mFuc-TIX, that synthesizes the Lewis x (CD15) epitope in brain and kidney. J Biol Chem. 1998;273(41):26729–38.

    CAS  PubMed  Google Scholar 

  • Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, et al. Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U S A. 2010;107(19):8639–43.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci U S A. 2000;97(25):13883–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Le Douarin NM, Teillet MA. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol. 1973;30(1):31–48.

    PubMed  Google Scholar 

  • Levine JM, Stallcup WB. Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J Neurosci. 1987;7(9):2721–31.

    CAS  PubMed  Google Scholar 

  • Ligon KL, Kesari S, Kitada M, Sun T, Arnett HA, Alberta JA, et al. Development of NG2 neural progenitor cells requires Olig gene function. Proc Natl Acad Sci U S A. 2006;103(20):7853–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lugert S, Vogt M, Tchorz JS, Muller M, Giachino C, Taylor V. Homeostatic neurogenesis in the adult hippocampus does not involve amplification of Ascl1(high) intermediate progenitors. Nat Commun. 2012;3:670.

    PubMed  Google Scholar 

  • Lui JH, Hansen DV, Kriegstein AR. Development and evolution of the human neocortex. Cell. 2011;146(1):18–36.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luther KB, Haltiwanger RS. Role of unusual O-glycans in intercellular signaling. Int J Biochem Cell Biol. 2009;41(5):1011–24.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mai JK, Andressen C, Ashwell KW. Demarcation of prosencephalic regions by CD15-positive radial glia. Eur J Neurosci. 1998;10(2):746–51.

    CAS  PubMed  Google Scholar 

  • Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, et al. Neuronal or glial progeny: regional differences in radial glia fate. Neuron. 2003;37(5):751–64.

    CAS  PubMed  Google Scholar 

  • Malatesta P, Hartfuss E, Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development. 2000;127(24):5253–63.

    CAS  PubMed  Google Scholar 

  • Margolis RK, Ripellino JA, Goossen B, Steinbrich R, Margolis RU. Occurrence of the HNK-1 epitope (3-sulfoglucuronic acid) in PC12 pheochromocytoma cells, chromaffin granule membranes, and chondroitin sulfate proteoglycans. Biochem Biophys Res Commun. 1987;145(3):1142–8.

    CAS  PubMed  Google Scholar 

  • Marzesco AM, Janich P, Wilsch-Brauninger M, Dubreuil V, Langenfeld K, Corbeil D, et al. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci. 2005;118(Pt 13):2849–58.

    CAS  PubMed  Google Scholar 

  • McCarthy M, Turnbull DH, Walsh CA, Fishell G. Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci. 2001;21(17):6772–81.

    CAS  PubMed  Google Scholar 

  • Mendez-Otero R, Cavalcante LA. Expression of 9-O-acetylated gangliosides is correlated with tangential cell migration in the rat brain. Neurosci Lett. 1996;204(1–2):97–100.

    CAS  PubMed  Google Scholar 

  • Mendez-Otero R, Schlosshauer B, Barnstable CJ, Constantine-Paton M. A developmentally regulated antigen associated with neural cell and process migration. J Neurosci. 1988;8(2):564–79.

    CAS  PubMed  Google Scholar 

  • Miller FD, Gauthier AS. Timing is everything: making neurons versus glia in the developing cortex. Neuron. 2007;54(3):357–69.

    CAS  PubMed  Google Scholar 

  • Miyakoshi LM, Todeschini AR, Mendez-Otero R, Hedin-Pereira C. Role of the 9-O-acetyl GD3 in subventricular zone neuroblast migration. Mol Cell Neurosci. 2012;49(2):240–9.

    CAS  PubMed  Google Scholar 

  • Miyata T, Kawaguchi A, Okano H, Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron. 2001;31(5):727–41.

    CAS  PubMed  Google Scholar 

  • Mizutani K, Yoon K, Dang L, Tokunaga A, Gaiano N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature. 2007;449(7160):351–5.

    CAS  PubMed  Google Scholar 

  • Mo Z, Moore AR, Filipovic R, Ogawa Y, Kazuhiro I, Antic SD, et al. Human cortical neurons originate from radial glia and neuron-restricted progenitors. J Neurosci. 2007;27(15):4132–45.

    CAS  PubMed  Google Scholar 

  • Moloney DJ, Shair LH, Lu FM, Xia J, Locke R, Matta KL, et al. Mammalian Notch1 is modified with two unusual forms of O-linked glycosylation found on epidermal growth factor-like modules. J Biol Chem. 2000;275(13):9604–11.

    CAS  PubMed  Google Scholar 

  • Morris-Wiman J, Brinkley LL. The role of the mesenchyme in mouse neural fold elevation. I. Patterns of mesenchymal cell distribution and proliferation in embryos developing in vitro. Am J Anat. 1990a;188(2):121–32.

    CAS  PubMed  Google Scholar 

  • Morris-Wiman J, Brinkley LL. The role of the mesenchyme in mouse neural fold elevation. II. Patterns of hyaluronate synthesis and distribution in embryos developing in vitro. Am J Anat. 1990b;188(2):133–47.

    CAS  PubMed  Google Scholar 

  • Morrison SJ, White PM, Zock C, Anderson DJ. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell. 1999;96(5):737–49.

    CAS  PubMed  Google Scholar 

  • Morshead CM. Adult neural stem cells: attempting to solve the identity crisis. Dev Neurosci. 2004;26(2–4):93–100.

    CAS  PubMed  Google Scholar 

  • Murakami K, Asou H, Adachi T, Takagi T, Kunimoto M, Saito H, et al. Neutral glycolipid and ganglioside composition of type-1 and type-2 astrocytes from rat cerebral hemisphere. J Neurosci Res. 1999;55(3):382–93.

    CAS  PubMed  Google Scholar 

  • Muramatsu T, Muramatsu H. Carbohydrate antigens expressed on stem cells and early embryonic cells. Glycoconj J. 2004;21(1–2):41–5.

    CAS  PubMed  Google Scholar 

  • Nagase T, Sanai Y, Nakamura S, Asato H, Harii K, Osumi N. Roles of HNK-1 carbohydrate epitope and its synthetic glucuronyltransferase genes on migration of rat neural crest cells. J Anat. 2003;203(1):77–88.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagatsuka Y, Hara-Yokoyama M, Kasama T, Takekoshi M, Maeda F, Ihara S, et al. Carbohydrate-dependent signaling from the phosphatidylglucoside-based microdomain induces granulocytic differentiation of HL60 cells. Proc Natl Acad Sci U S A. 2003;100(13):7454–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagatsuka Y, Horibata Y, Yamazaki Y, Kinoshita M, Shinoda Y, Hashikawa T, et al. Phosphatidylglucoside exists as a single molecular species with saturated fatty acyl chains in developing astroglial membranes. Biochemistry. 2006;45(29):8742–50.

    CAS  PubMed  Google Scholar 

  • Nagatsuka Y, Kasama T, Ohashi Y, Uzawa J, Ono Y, Shimizu K, et al. A new phosphoglycerolipid, “phosphatidylglucose,” found in human cord red cells by multi-reactive monoclonal anti-i cold agglutinin, mAb GL-1/GL-2. FEBS Lett. 2001;497(2–3):141–7.

    CAS  PubMed  Google Scholar 

  • Nakashima K, Wiese S, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, et al. Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J Neurosci. 1999a;19(13):5429–34.

    CAS  PubMed  Google Scholar 

  • Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science. 1999b;284(5413):479–82.

    CAS  PubMed  Google Scholar 

  • Nakatani Y, Yanagisawa M, Suzuki Y, Yu RK. Characterization of GD3 ganglioside as a novel biomarker of mouse neural stem cells. Glycobiology. 2010;20(1):78–86.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ngamukote S, Yanagisawa M, Ariga T, Ando S, Yu RK. Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J Neurochem. 2007;103(6):2327–41.

    CAS  PubMed  Google Scholar 

  • Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. Neurons derived from radial glial cells establish radial units in neocortex. Nature. 2001;409(6821):714–20.

    CAS  PubMed  Google Scholar 

  • Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci. 2002;22(8):3161–73.

    CAS  PubMed  Google Scholar 

  • Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 2004;7(2):136–44.

    CAS  PubMed  Google Scholar 

  • Ogura K, Kohno K, Tai T. Molecular cloning of a rat brain cDNA, with homology to a tyrosine kinase substrate, that induces galactosylceramide expression in COS-7 cells. J Neurochem. 1998;71(5):1827–36.

    CAS  PubMed  Google Scholar 

  • Ogura K, Tai T. Molecular cloning and characterization of galactosylceramide expression factor-1 (GEF-1). Neurochem Res. 2002;27(7–8):779–84.

    CAS  PubMed  Google Scholar 

  • Okajima T, Irvine KD. Regulation of notch signaling by o-linked fucose. Cell. 2002;111(6):893–904.

    CAS  PubMed  Google Scholar 

  • Okajima T, Matsuura A, Matsuda T. Biological functions of glycosyltransferase genes involved in O-fucose glycan synthesis. J Biochem. 2008;144(1):1–6.

    CAS  PubMed  Google Scholar 

  • Okajima T, Xu A, Irvine KD. Modulation of notch-ligand binding by protein O-fucosyltransferase 1 and fringe. J Biol Chem. 2003;278(43):42340–5.

    CAS  PubMed  Google Scholar 

  • Okajima T, Xu A, Lei L, Irvine KD. Chaperone activity of protein O-fucosyltransferase 1 promotes notch receptor folding. Science. 2005;307(5715):1599–603.

    CAS  PubMed  Google Scholar 

  • Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T. Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res. 2005;306(2):349–56.

    CAS  PubMed  Google Scholar 

  • Okuda T, Tokuda N, Numata S, Ito M, Ohta M, Kawamura K, et al. Targeted disruption of Gb3/CD77 synthase gene resulted in the complete deletion of globo-series glycosphingolipids and loss of sensitivity to verotoxins. J Biol Chem. 2006;281(15):10230–5.

    CAS  PubMed  Google Scholar 

  • Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci. 1999;19(19):8487–97.

    CAS  PubMed  Google Scholar 

  • Panin VM, Papayannopoulos V, Wilson R, Irvine KD. Fringe modulates Notch-ligand interactions. Nature. 1997;387(6636):908–12.

    CAS  PubMed  Google Scholar 

  • Petridis AK, El-Maarouf A, Rutishauser U. Polysialic acid regulates cell contact-dependent neuronal differentiation of progenitor cells from the subventricular zone. Dev Dyn. 2004 Aug;230(4):675–84.

    Google Scholar 

  • Pettway Z, Domowicz M, Schwartz NB, Bronner-Fraser M. Age-dependent inhibition of neural crest migration by the notochord correlates with alterations in the S103L chondroitin sulfate proteoglycan. Exp Cell Res. 1996;225(1):195–206.

    CAS  PubMed  Google Scholar 

  • Pinto L, Gotz M. Radial glial cell heterogeneity – the source of diverse progeny in the CNS. Prog Neurobiol. 2007;83(1):2–23.

    CAS  PubMed  Google Scholar 

  • Purves D, Lichtman JW. Principles of neural development. Sunderland, MA: Sinauer Associates; 1985.

    Google Scholar 

  • Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, et al. Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron. 2000;28(1):69–80.

    CAS  PubMed  Google Scholar 

  • Raff MC, Abney ER, Cohen J, Lindsay R, Noble M. Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J Neurosci. 1983a;3(6):1289–300.

    CAS  PubMed  Google Scholar 

  • Raff MC, Miller RH, Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature. 1983b;303(5916):390–6.

    CAS  PubMed  Google Scholar 

  • Rao MS, Mayer-Proschel M. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol. 1997;188(1):48–63.

    CAS  PubMed  Google Scholar 

  • Reijo Pera RA, DeJonge C, Bossert N, Yao M, Hwa Yang JY, Asadi NB, et al. Gene expression profiles of human inner cell mass cells and embryonic stem cells. Differentiation. 2009;78(1):18–23.

    PubMed  Google Scholar 

  • Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255(5052):1707–10.

    CAS  PubMed  Google Scholar 

  • Richardson WD, Young KM, Tripathi RB, McKenzie I. NG2-glia as multipotent neural stem cells: fact or fantasy? Neuron. 2011;70(4):661–73.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature. 2001;412(6848):736–9.

    CAS  PubMed  Google Scholar 

  • Roper K, Corbeil D, Huttner WB. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol. 2000;2(9):582–92.

    CAS  PubMed  Google Scholar 

  • Rosner H, al-Aqtum M, Rahmann H. Gangliosides and neuronal differentiation. Neurochem Int. 1992;20(3):339–51.

    CAS  PubMed  Google Scholar 

  • Rosner H, Greis C, Henke-Fahle S. Developmental expression in embryonic rat and chicken brain of a polysialoganglioside-antigen reacting with the monoclonal antibody Q 211. Brain Res. 1988;470(2):161–71.

    CAS  PubMed  Google Scholar 

  • Rowitch DH, Kriegstein AR. Developmental genetics of vertebrate glial-cell specification. Nature. 2010;468(7321):214–22.

    CAS  PubMed  Google Scholar 

  • Rutishauser U, Landmesser L. Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell–cell interactions. Trends Neurosci. 1996;19(10):422–7.

    CAS  PubMed  Google Scholar 

  • Saito M, Kitamura H, Sugiyama K. The specificity of monoclonal antibody A2B5 to c-series gangliosides. J Neurochem. 2001;78(1):64–74.

    CAS  PubMed  Google Scholar 

  • Sasamura T, Sasaki N, Miyashita F, Nakao S, Ishikawa HO, Ito M, et al. Neurotic, a novel maternal neurogenic gene, encodes an O-fucosyltransferase that is essential for Notch-Delta interactions. Development. 2003;130(20):4785–95.

    CAS  PubMed  Google Scholar 

  • Sauka-Spengler T, Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol. 2008;9(7):557–68.

    CAS  PubMed  Google Scholar 

  • Sbaschnig-Agler M, Dreyfus H, Norton WT, Sensenbrenner M, Farooq M, Byrne MC, et al. Gangliosides of cultured astroglia. Brain Res. 1988;461(1):98–106.

    CAS  PubMed  Google Scholar 

  • Schoenwolf GC, Fisher M. Analysis of the effects of Streptomyces hyaluronidase on formation of the neural tube. J Embryol Exp Morphol. 1983;73:1–15.

    CAS  PubMed  Google Scholar 

  • 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. 1998;18(10):3757–66.

    CAS  PubMed  Google Scholar 

  • Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 2001;21(18):7153–60.

    CAS  PubMed  Google Scholar 

  • Shah NM, Groves AK, Anderson DJ. Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell. 1996;85(3):331–43.

    CAS  PubMed  Google Scholar 

  • Shah NM, Marchionni MA, Isaacs I, Stroobant P, Anderson DJ. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell. 1994;77(3):349–60.

    CAS  PubMed  Google Scholar 

  • Sharon N. Lectins: past, present and future. Biochem Soc Trans. 2008;36(Pt 6):1457–60.

    CAS  PubMed  Google Scholar 

  • Sharon N, Lis H. Lectins: cell-agglutinating and sugar-specific proteins. Science. 1972;177(4053):949–59.

    CAS  PubMed  Google Scholar 

  • Sheikh KA, Sun J, Liu Y, Kawai H, Crawford TO, Proia RL, et al. Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc Natl Acad Sci U S A. 1999;96(13):7532–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shi S, Stanley P. Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc Natl Acad Sci U S A. 2003;100(9):5234–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shimazaki T, Shingo T, Weiss S. The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci. 2001;21(19):7642–53.

    CAS  PubMed  Google Scholar 

  • Shimojo H, Ohtsuka T, Kageyama R. Dynamic expression of notch signaling genes in neural stem/progenitor cells. Front Neurosci. 2011;5:78.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shmelkov SV, St Clair R, Lyden D, Rafii S. AC133/CD133/Prominin-1. Int J Biochem Cell Biol. 2005;37(4):715–9.

    CAS  PubMed  Google Scholar 

  • Sieber-Blum M. Commitment of neural crest cells to the sensory neuron lineage. Science. 1989;243(4898):1608–11.

    CAS  PubMed  Google Scholar 

  • Simpson MA, Cross H, Proukakis C, Priestman DA, Neville DC, Reinkensmeier G, et al. Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat Genet. 2004;36(11):1225–9.

    CAS  PubMed  Google Scholar 

  • Singh RD, Schroeder AS, Scheffer L, Holicky EL, Wheatley CL, Marks DL, et al. Prominin-2 expression increases protrusions, decreases caveolae and inhibits Cdc42 dependent fluid phase endocytosis. Biochem Biophys Res Commun. 2013;434(3):466–72.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Skaggs K, Martin DM, Novitch BG. Regulation of spinal interneuron development by the Olig-related protein Bhlhb5 and Notch signaling. Development. 2011;138(15):3199–211.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smart IH. Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J Anat. 1973;116(Pt 1):67–91.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Solter D, Knowles BB. Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci U S A. 1978;75(11):5565–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stainier DY, Bilder DH, Gilbert W. The B30 ganglioside is a cell surface marker for neural crest-derived neurons in the developing mouse. Dev Biol. 1991;144(1):177–88.

    CAS  PubMed  Google Scholar 

  • Stallcup WB. The NG2 antigen, a putative lineage marker: immunofluorescent localization in primary cultures of rat brain. Dev Biol. 1981;83(1):154–65.

    CAS  PubMed  Google Scholar 

  • Stanley P, Okajima T. Roles of glycosylation in Notch signaling. Curr Top Dev Biol. 2010;92:131–64.

    CAS  PubMed  Google Scholar 

  • Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia. 2006;54(8):805–14.

    PubMed  Google Scholar 

  • Stemple DL, Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell. 1992;71(6):973–85.

    CAS  PubMed  Google Scholar 

  • Sugiura Y, Furukawa K, Tajima O, Mii S, Honda T. Sensory nerve-dominant nerve degeneration and remodeling in the mutant mice lacking complex gangliosides. Neuroscience. 2005;135(4):1167–78.

    CAS  PubMed  Google Scholar 

  • Suhonen JO, Peterson DA, Ray J, Gage FH. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature. 1996;383(6601):624–7.

    CAS  PubMed  Google Scholar 

  • Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, et al. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell. 2001;104(3):365–76.

    CAS  PubMed  Google Scholar 

  • Susuki K, Baba H, Tohyama K, Kanai K, Kuwabara S, Hirata K, et al. Gangliosides contribute to stability of paranodal junctions and ion channel clusters in myelinated nerve fibers. Glia. 2007;55(7):746–57.

    PubMed  Google Scholar 

  • Svennerholm L. Chromatographic separation of human brain gangliosides. J Neurochem. 1963;10:613–23.

    CAS  PubMed  Google Scholar 

  • Taga T, Hibi M, Hirata Y, Yamasaki K, Yasukawa K, Matsuda T, et al. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell. 1989;58(3):573–81.

    CAS  PubMed  Google Scholar 

  • Takamiya K, Yamamoto A, Furukawa K, Yamashiro S, Shin M, Okada M, et al. Mice with disrupted GM2/GD2 synthase gene lack complex gangliosides but exhibit only subtle defects in their nervous system. Proc Natl Acad Sci U S A. 1996;93(20):10662–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell. 2001;1(6):749–58.

    CAS  PubMed  Google Scholar 

  • Thallmair M, Ray J, Stallcup WB, Gage FH. Functional and morphological effects of NG2 proteoglycan deletion on hippocampal neurogenesis. Exp Neurol. 2006;202(1):167–78.

    CAS  PubMed  Google Scholar 

  • Tokuda A, Ariga T, Isogai Y, Komba S, Kiso M, Hasegawa A, et al. On the specificity of anti-sulfoglucuronosyl glycolipid antibodies’. J Carbohyd Chem. 1998;17(4–5):535–46.

    CAS  Google Scholar 

  • Tole S, Kaprielian Z, Ou SK, Patterson PH. FORSE-1: a positionally regulated epitope in the developing rat central nervous system. J Neurosci. 1995;15(2):957–69.

    CAS  PubMed  Google Scholar 

  • Tucker GC, Delarue M, Zada S, Boucaut JC, Thiery JP. Expression of the HNK-1/NC-1 epitope in early vertebrate neurogenesis. Cell Tissue Res. 1988;251(2):457–65.

    CAS  PubMed  Google Scholar 

  • von Holst A, Sirko S, Faissner A. The unique 473HD-Chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci. 2006;26(15):4082–94.

    Google Scholar 

  • Wakao S, Kitada M, Kuroda Y, Shigemoto T, Matsuse D, Akashi H, et al. Multilineage-differentiating stress-enduring (Muse) cells are a primary source of induced pluripotent stem cells in human fibroblasts. Proc Natl Acad Sci U S A. 2011;108(24):9875–80.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Walker TL, Wierick A, Sykes AM, Waldau B, Corbeil D, Carmeliet P, et al. Prominin-1 allows prospective isolation of neural stem cells from the adult murine hippocampus. J Neurosci. 2013;33(7):3010–24.

    CAS  PubMed  Google Scholar 

  • Walters LC, Cantrell VA, Weller KP, Mosher JT, Southard-Smith EM. Genetic background impacts developmental potential of enteric neural crest-derived progenitors in the Sox10Dom model of Hirschsprung disease. Hum Mol Genet. 2010;19(22):4353–72.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weigmann A, Corbeil D, Hellwig A, Huttner WB. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci U S A. 1997;94(23):12425–30.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu G, Fang Y, Lu ZH, Ledeen RW. Induction of axon-like and dendrite-like processes in neuroblastoma cells. J Neurocytol. 1998;27(1):1–14.

    CAS  PubMed  Google Scholar 

  • Wu G, Lu ZH, Kulkarni N, Amin R, Ledeen RW. Mice lacking major brain gangliosides develop parkinsonism. Neurochem Res. 2011;36(9):1706–14.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu G, Lu ZH, Xie X, Li L, Ledeen RW. Mutant NG108-15 cells (NG-CR72) deficient in GM1 synthase respond aberrantly to axonogenic stimuli and are vulnerable to calcium-induced apoptosis: they are rescued with LIGA-20. J Neurochem. 2001;76(3):690–702.

    CAS  PubMed  Google Scholar 

  • Yagi H, Saito T, Yanagisawa M, Yu RK, Kato K. Lewis X-carrying N-glycans regulate the proliferation of mouse embryonic neural stem cells via the Notch signaling pathway. J Biol Chem. 2012;287(29):24356–64.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yagi H, Yanagisawa M, Kato K, Yu RK. Lysosome-associated membrane protein 1 is a major SSEA-1-carrier protein in mouse neural stem cells. Glycobiology. 2010a;20(8):976–81.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yagi H, Yanagisawa M, Suzuki Y, Nakatani Y, Ariga T, Kato K, et al. HNK-1 epitope-carrying tenascin-C spliced variant regulates the proliferation of mouse embryonic neural stem cells. J Biol Chem. 2010b;285(48):37293–301.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto N, Inui K, Matsuyama Y, Harada A, Hanamura K, Murakami F, et al. Inhibitory mechanism by polysialic acid for lamina-specific branch formation of thalamocortical axons. J Neurosci. 2000 Dec 15;20(24):9145–51.

    Google Scholar 

  • Yamamoto S, Oka S, Inoue M, Shimuta M, Manabe T, Takahashi H, et al. Mice deficient in nervous system-specific carbohydrate epitope HNK-1 exhibit impaired synaptic plasticity and spatial learning. J Biol Chem. 2002;277(30):27227–31.

    CAS  PubMed  Google Scholar 

  • Yamashita T, Wada R, Sasaki T, Deng C, Bierfreund U, Sandhoff K, et al. A vital role for glycosphingolipid synthesis during development and differentiation. Proc Natl Acad Sci U S A. 1999;96(16):9142–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yanagisawa M, Liour SS, Yu RK. Involvement of gangliosides in proliferation of immortalized neural progenitor cells. J Neurochem. 2004a;91(4):804–12.

    CAS  PubMed  Google Scholar 

  • Yanagisawa M, Nakamura K, Taga T. Roles of lipid rafts in integrin-dependent adhesion and gp130 signalling pathway in mouse embryonic neural precursor cells. Genes Cells. 2004b;9(9):801–9.

    CAS  PubMed  Google Scholar 

  • Yanagisawa M, Taga T, Nakamura K, Ariga T, Yu RK. Characterization of glycoconjugate antigens in mouse embryonic neural precursor cells. J Neurochem. 2005;95(5):1311–20.

    CAS  PubMed  Google Scholar 

  • Yanagisawa M, Yu RK. The expression and functions of glycoconjugates in neural stem cells. Glycobiology. 2007;17(7):57R–74.

    CAS  PubMed  Google Scholar 

  • Yanagisawa M, Yu RK. N-glycans modulate the activation of gp130 in mouse embryonic neural precursor cells. Biochem Biophys Res Commun. 2009;386(1):101–4.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang CR, Liour SS, Dasgupta S, Yu RK. Inhibition of neuronal migration by JONES antibody is independent of 9-O-acetyl GD3 in GD3-synthase knockout mice. J Neurosci Res. 2007;85(7):1381–90.

    CAS  PubMed  Google Scholar 

  • Yu RK, Ando S. Structures of some new complex gangliosides of fish brain. Adv Exp Med Biol. 1980;125:33–45.

    CAS  PubMed  Google Scholar 

  • Yu RK, Bieberich E, Xia T, Zeng G. Regulation of ganglioside biosynthesis in the nervous system. J Lipid Res. 2004;45(5):783–93.

    CAS  PubMed  Google Scholar 

  • Yu RK, Macala LJ, Taki T, Weinfield HM, Yu FS. Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem. 1988;50(6):1825–9.

    CAS  PubMed  Google Scholar 

  • Yu RK, Nakatani Y, Yanagisawa M. The role of glycosphingolipid metabolism in the developing brain. J Lipid Res. 2009;50(Suppl):S440–5.

    PubMed Central  PubMed  Google Scholar 

  • Yu RK, Tsai YT, Ariga T. Functional roles of gangliosides in neurodevelopment: an overview of recent advances. Neurochem Res. 2012;37(6):1230–44.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zacchigna S, Oh H, Wilsch-Brauninger M, Missol-Kolka E, Jaszai J, Jansen S, et al. Loss of the cholesterol-binding protein prominin-1/CD133 causes disk dysmorphogenesis and photoreceptor degeneration. J Neurosci. 2009;29(7):2297–308.

    CAS  PubMed  Google Scholar 

  • Zhang SC. Defining glial cells during CNS development. Nat Rev Neurosci. 2001;2(11):840–3.

    CAS  PubMed  Google Scholar 

  • Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development. 2011;138(4):745–53.

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Conflict of Interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert K. Yu .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Yu, R.K., Itokazu, Y. (2014). Glycolipid and Glycoprotein Expression During Neural Development. In: Yu, R., Schengrund, CL. (eds) Glycobiology of the Nervous System. Advances in Neurobiology, vol 9. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1154-7_9

Download citation

Publish with us

Policies and ethics