Skip to main content
SpringerLink
Log in
Book cover

Glycobiology of the Nervous System pp 89–115Cite as

Chemistry and Function of Glycosaminoglycans in the Nervous System

  • Chapter
  • First Online:

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

Abstract

The glycosaminoglycan (GAG) family is characterized by covalently linked repeating disaccharides forming long unbranched polysaccharide chains. Thus far in higher eukaryotes, the family consists of chondroitin sulfate (CS), heparin/heparan sulfate (HS), dermatan sulfate (DS), and hyaluronan (HA). All GAG chains (except HA) are characteristically modified by varying amounts of esterified sulfate. One or more GAG chains are usually found in nature bound to polypeptide backbones in the form of proteoglycans; HA is the exception and is not synthesized covalently bound to a protein. Proteoglycans, and especially their GAG components, participate in numerous biologically significant interactions with growth factors, chemokines, morphogens, guidance molecules, survival factors, and other extracellular and cell-surface components. These interactions are often critical to the basic developmental processes of cellular proliferation and differentiation, as well as to both the onset of disease sequelae and the prevention of disease progression. In the nervous system, GAG/proteoglycan-mediated interactions participate in proliferation and synaptogenesis, neural plasticity, and regeneration. This review focuses on the structure, chemistry, and function of GAGs in nervous system development, disease, and injury response.

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

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

APP:

β-Amyloid precursor protein

CS:

Chondroitin sulfate

DS:

Dermatan sulfate

Ext1:

Exostosin glycosyltransferase 1

FGF:

Fibroblast growth factor

GAG:

Glycosaminoglycan

Gal:

Galactose

GalNAc:

N-Acetylgalactosamine

GalNAc4S6ST:

N-Acetylgalactosamine 4-sulfate 6-O-sulfotransferase

Gdf5:

Growth differentiation factor 5

GlcA:

Glucuronic acid

GlcAT-1:

Glucuronosyltransferase-I

GlcN:

Glucosamine

GlcNAc:

N-Acetylglucosamine

HA:

Hyaluronan

HS:

Heparan sulfate

IdoA:

Iduronic acid

LAR:

Leukocyte common antigen-related phosphatase

NDST:

N-Deacetylase/N-sulfotransferases

NSC:

Neural stem cell

PAPS:

3′-Phosphoadenosyl 5′-phosphosulfate

PNN:

Perineuronal net

VZ:

Ventricular zone

References

  • Akatsu C, Mizumoto S, Kaneiwa T, Maccarana M, Malmstrom A, Yamada S, et al. Dermatan sulfate epimerase 2 is the predominant isozyme in the formation of the chondroitin sulfate/dermatan sulfate hybrid structure in postnatal developing mouse brain. Glycobiology. 2011;21(5):565–74.

    CAS  PubMed  Google Scholar 

  • Akita K, von Holst A, Furukawa Y, Mikami T, Sugahara K, Faissner A. Expression of multiple chondroitin/dermatan sulfotransferases in the neurogenic regions of the embryonic and adult central nervous system implies that complex chondroitin sulfates have a role in neural stem cell maintenance. Stem Cells. 2008;26(3):798–809.

    CAS  PubMed  Google Scholar 

  • Ariga T, Miyatake T, Yu RK. Role of proteoglycans and glycosaminoglycans in the pathogenesis of Alzheimer’s disease and related disorders: amyloidogenesis and therapeutic strategies–a review. J Neurosci Res. 2010;88(11):2303–15.

    CAS  PubMed  Google Scholar 

  • Ashikari-Hada S, Habuchi H, Kariya Y, Itoh N, Reddi AH, Kimata K. Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J Biol Chem. 2004;279(13):12346–54.

    CAS  PubMed  Google Scholar 

  • Back SA, Tuohy TM, Chen H, Wallingford N, Craig A, Struve J, et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat Med. 2005;11(9):966–72.

    CAS  PubMed  Google Scholar 

  • Bandtlow CE, Zimmermann DR. Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev. 2000;80(4):1267–90.

    CAS  PubMed  Google Scholar 

  • Banecka-Majkutewicz Z, Jakobkiewicz-Banecka J, Gabig-Ciminska M, Wegrzyn A, Wegrzyn G. Putative biological mechanisms of efficiency of substrate reduction therapies for mucopolysaccharidoses. Arch Immunol Ther Exp (Warsz). 2012;60(6):461–8.

    CAS  Google Scholar 

  • Bao X, Mikami T, Yamada S, Faissner A, Muramatsu T, Sugahara K. Heparin-binding growth factor, pleiotrophin, mediates neuritogenic activity of embryonic pig brain-derived chondroitin sulfate/dermatan sulfate hybrid chains. J Biol Chem. 2005;280(10):9180–91.

    CAS  PubMed  Google Scholar 

  • Beckman M, Holsinger RM, Small DH. Heparin activates beta-secretase (BACE1) of Alzheimer’s disease and increases autocatalysis of the enzyme. Biochemistry. 2006;45(21):6703–14.

    CAS  PubMed  Google Scholar 

  • Bornemann DJ, Park S, Phin S, Warrior R. A translational block to HSPG synthesis permits BMP signaling in the early Drosophila embryo. Development. 2008;135(6):1039–47.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bradbury EJ, Carter LM. Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Res Bull. 2011;84(4–5):306–16.

    CAS  PubMed  Google Scholar 

  • Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 2002;416(6881):636–40.

    CAS  PubMed  Google Scholar 

  • Brakebusch C, Seidenbecher CI, Asztely F, Rauch U, Matthies H, Meyer H, et al. Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol. 2002;22(21):7417–27.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brittis PA, Canning DR, Silver J. Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science. 1992;255:733–6.

    CAS  PubMed  Google Scholar 

  • Bukalo O, Schachner M, Dityatev A. Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience. 2001;104(2):359–69.

    CAS  PubMed  Google Scholar 

  • Cafferty WB, Yang SH, Duffy PJ, Li S, Strittmatter SM. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci. 2007;27(9):2176–85.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carter LM, McMahon SB, Bradbury EJ. Delayed treatment with chondroitinase ABC reverses chronic atrophy of rubrospinal neurons following spinal cord injury. Exp Neurol. 2011;228(1):149–56.

    CAS  PubMed  Google Scholar 

  • Carulli D, Laabs T, Geller HM, Fawcett JW. Chondroitin sulfate proteoglycans in neural development and regeneration. Curr Opin Neurobiol. 2005;15(1):116–20.

    PubMed  Google Scholar 

  • Carulli D, Pizzorusso T, Kwok JC, Putignano E, Poli A, Forostyak S, et al. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain. 2010;133(Pt 8):2331–47.

    PubMed  Google Scholar 

  • Cho JY, Chak K, Andreone BJ, Wooley JR, Kolodkin AL. The extracellular matrix proteoglycan perlecan facilitates transmembrane semaphorin-mediated repulsive guidance. Genes Dev. 2012;26(19):2222–35.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chung KY, Shum DK, Chan SO. Expression of chondroitin sulfate proteoglycans in the chiasm of mouse embryos. J Comp Neurol. 2000a;417(2):153–63.

    CAS  PubMed  Google Scholar 

  • Chung KY, Taylor JS, Shum DK, Chan SO. Axon routing at the optic chiasm after enzymatic removal of chondroitin sulfate in mouse embryos. Development. 2000b;127(12):2673–83.

    CAS  PubMed  Google Scholar 

  • Crespo D, Asher RA, Lin R, Rhodes KE, Fawcett JW. How does chondroitinase promote functional recovery in the damaged CNS? Exp Neurol. 2007;206(2):159–71.

    CAS  PubMed  Google Scholar 

  • Cua RC, Lau LW, Keough MB, Midha R, Apte SS, Yong VW. Overcoming neurite-inhibitory chondroitin sulfate proteoglycans in the astrocyte matrix. Glia. 2013;61(6):972–84.

    PubMed  Google Scholar 

  • Cui H, Hung AC, Freeman C, Narkowicz C, Jacobson GA, Small DH. Size and sulfation are critical for the effect of heparin on APP processing and Abeta production. J Neurochem. 2012;123(3):447–57.

    CAS  PubMed  Google Scholar 

  • Cui H, Freeman C, Jacobson GA, Small DH. Proteoglycans in the central nervous system: role in development, neural repair, and Alzheimer’s disease. IUBMB Life. 2013;65(2):108–20.

    CAS  PubMed  Google Scholar 

  • Deak A, Bacskai T, Gaal B, Racz E, Matesz K. Effect of unilateral labyrinthectomy on the molecular composition of perineuronal nets in the lateral vestibular nucleus of the rat. Neurosci Lett. 2012;513(1):1–5.

    CAS  PubMed  Google Scholar 

  • Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K. Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem. 2002;277(46):43707–16.

    CAS  PubMed  Google Scholar 

  • Deepa SS, Carulli D, Galtrey C, Rhodes K, Fukuda J, Mikami T, et al. Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J Biol Chem. 2006;281(26):17789–800.

    CAS  PubMed  Google Scholar 

  • Dickendesher TL, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, Askew KL, et al. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci. 2012;15(5):703–12.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Domowicz MS, Sanders TA, Ragsdale CW, Schwartz NB. Aggrecan is expressed by embryonic brain glia and regulates astrocyte development. Dev Biol. 2008;315(1):114–24.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dudas B, Semeniken K. Glycosaminoglycans and neuroprotection. Handb Exp Pharmacol. 2012;207:325–43.

    CAS  PubMed  Google Scholar 

  • Dundar M, Muller T, Zhang Q, Pan J, Steinmann B, Vodopiutz J, et al. Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome. Am J Hum Genet. 2009;85(6):873–82.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ethell IM, Yamaguchi Y. Cell surface heparan sulfate proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J Cell Biol. 1999;144(3):575–86.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fawcett J. Molecular control of brain plasticity and repair. Prog Brain Res. 2009;175:501–9.

    CAS  PubMed  Google Scholar 

  • Fernaud-Espinosa I, Nieto-Sampedro M, Bovolenta P. Differential effects of glycosaminoglycans on neurite outgrowth from hippocampal and thalamic neurones. J Cell Sci. 1994;107(Pt 6):1437–48.

    CAS  PubMed  Google Scholar 

  • Fisher D, Xing B, Dill J, Li H, Hoang HH, Zhao Z, et al. Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci. 2011;31(40):14051–66.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fitch MT, Silver J. Glial cell extracellular matrix: boundaries for axon growth in development and regeneration. Cell Tissue Res. 1997;290(2):379–84.

    CAS  PubMed  Google Scholar 

  • Ford-Perriss M, Turner K, Guimond S, Apedaile A, Haubeck HD, Turnbull J, et al. Localisation of specific heparan sulfate proteoglycans during the proliferative phase of brain development. Dev Dyn. 2003;227(2):170–84.

    CAS  PubMed  Google Scholar 

  • Frischknecht R, Gundelfinger ED. The brain’s extracellular matrix and its role in synaptic plasticity. Adv Exp Med Biol. 2012;970:153–71.

    CAS  PubMed  Google Scholar 

  • Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci. 2009;12(7):897–904.

    CAS  PubMed  Google Scholar 

  • Galtrey CM, Fawcett JW. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev. 2007;54(1):1–18.

    CAS  PubMed  Google Scholar 

  • Galtrey CM, Asher RA, Nothias F, Fawcett JW. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain. 2007;130(Pt 4):926–39.

    PubMed  Google Scholar 

  • Galtrey CM, Kwok JC, Carulli D, Rhodes KE, Fawcett JW. Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur J Neurosci. 2008;27(6):1373–90.

    PubMed  Google Scholar 

  • Garcia-Alias G, Petrosyan HA, Schnell L, Horner PJ, Bowers WJ, Mendell LM, et al. Chondroitinase ABC combined with neurotrophin NT-3 secretion and NR2D expression promotes axonal plasticity and functional recovery in rats with lateral hemisection of the spinal cord. J Neurosci. 2011;31(49):17788–99.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giros A, Morante J, Gil-Sanz C, Fairen A, Costell M. Perlecan controls neurogenesis in the developing telencephalon. BMC Dev Biol. 2007;7:29.

    PubMed Central  PubMed  Google Scholar 

  • Goossens D, Van Gestel S, Claes S, De Rijk P, Souery D, Massat I, et al. A novel CpG-associated brain-expressed candidate gene for chromosome 18q-linked bipolar disorder. Mol Psychiatry. 2003;8(1):83–9.

    CAS  PubMed  Google Scholar 

  • Grobe K, Inatani M, Pallerla SR, Castagnola J, Yamaguchi Y, Esko JD. Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function. Development. 2005;132(16):3777–86.

    CAS  PubMed  Google Scholar 

  • Grumet M, Friedlander DR, Sakurai T. Functions of brain chondroitin sulfate proteoglycans during developments: interactions with adhesion molecules. Perspect Dev Neurobiol. 1996;3(4):319–30.

    CAS  PubMed  Google Scholar 

  • Gu W-L, Fu S-L, Wang Y-X, Li Y, Lu H-Z, Xu X-M, et al. Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway. BMC Neurosci. 2009;10:128.

    PubMed Central  PubMed  Google Scholar 

  • Haerry TE, Heslip TR, Marsh JL, O’Connor MB. Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila. Development. 1997;124(16):3055–64.

    CAS  PubMed  Google Scholar 

  • Hagihara K, Watanabe K, Chun J, Yamaguchi Y. Glypican-4 is an FGF2-binding heparan sulfate proteoglycan expressed in neural precursor cells. Dev Dyn. 2000;219(3):353–67.

    CAS  PubMed  Google Scholar 

  • Hagino S, Iseki K, Mori T, Zhang Y, Hikake T, Yokoya S, et al. Slit and glypican-1 mRNAs are coexpressed in the reactive astrocytes of the injured adult brain. Glia. 2003a;42(2):130–8.

    PubMed  Google Scholar 

  • Hagino S, Iseki K, Mori T, Zhang Y, Sakai N, Yokoya S, et al. Expression pattern of glypican-1 mRNA after brain injury in mice. Neurosci Lett. 2003b;349(1):29–32.

    CAS  PubMed  Google Scholar 

  • Hebert JM, Lin M, Partanen J, Rossant J, McConnell SK. FGF signaling through FGFR1 is required for olfactory bulb morphogenesis. Development. 2003;130(6):1101–11.

    CAS  PubMed  Google Scholar 

  • Hikino M, Mikami T, Faissner A, Vilela-Silva AC, Pavao MS, Sugahara K. Oversulfated dermatan sulfate exhibits neurite outgrowth-promoting activity toward embryonic mouse hippocampal neurons: implications of dermatan sulfate in neuritogenesis in the brain. J Biol Chem. 2003;278(44):43744–54.

    CAS  PubMed  Google Scholar 

  • Hill JJ, Jin K, Mao XO, Xie L, Greenberg DA. Intracerebral chondroitinase ABC and heparan sulfate proteoglycan glypican improve outcome from chronic stroke in rats. Proc Natl Acad Sci U S A. 2012;109(23):9155–60.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hoffman-Kim D, Lander AD, Jhaveri S. Patterns of chondroitin sulfate immunoreactivity in the developing tectum reflect regional differences in glycosaminoglycan biosynthesis. J Neurosci. 1998;18(15):5881–90.

    CAS  PubMed  Google Scholar 

  • Hughes GR. Heparin, antiphospholipid antibodies and the brain. Lupus. 2012;21(10):1039–40.

    CAS  PubMed  Google Scholar 

  • Ichijo H, Kawabata I. Roles of the telencephalic cells and their chondroitin sulfate proteoglycans in delimiting an anterior border of the retinal pathway. J Neurosci. 2001;21(23):9304–14.

    CAS  PubMed  Google Scholar 

  • Ida M, Shuo T, Hirano K, Tokita Y, Nakanishi K, Matsui F, et al. Identification and functions of chondroitin sulfate in the milieu of neural stem cells. J Biol Chem. 2006;281(9):5982–91.

    CAS  PubMed  Google Scholar 

  • Inatani M, Irie F, Plump AS, Tessier-Lavigne M, Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science. 2003;302(5647):1044–6.

    CAS  PubMed  Google Scholar 

  • Irie F, Yamaguchi Y. EPHB receptor signaling in dendritic spine development. Front Biosci. 2004;9:1365–73.

    CAS  PubMed  Google Scholar 

  • Irie F, Badie-Mahdavi H, Yamaguchi Y. Autism-like socio-communicative deficits and stereotypies in mice lacking heparan sulfate. Proc Natl Acad Sci U S A. 2012;109(13):5052–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iseki K, Hagino S, Zhang Y, Mori T, Sato N, Yokoya S, et al. Altered expression pattern of testican-1 mRNA after brain injury. Biomed Res. 2011;32(6):373–8.

    CAS  PubMed  Google Scholar 

  • Iseki K, Hagino S, Nikaido T, Zhang Y, Mori T, Yokoya S, et al. Gliosis-specific transcription factor OASIS coincides with proteoglycan core protein genes in the glial scar and inhibits neurite outgrowth. Biomed Res. 2012;33(6):345–53.

    CAS  PubMed  Google Scholar 

  • Ishii M. Maeda N. Glycobiology: Spatiotemporal expression of chondroitin sulfate sulfotransferases in the postnatal developing mouse cerebellum; 2008.

    Google Scholar 

  • Izumikawa T, Kitagawa H. Mice deficient in glucuronyltransferase-I. Prog Mol Biol Transl Sci. 2010;93:19–34.

    CAS  PubMed  Google Scholar 

  • Izumikawa T, Okuura Y, Koike T, Sakoda N, Kitagawa H. Chondroitin 4-O-sulfotransferase-1 regulates the chain length of chondroitin sulfate in co-operation with chondroitin N-acetylgalactosaminyltransferase-2. Biochem J. 2011;434(2):321–31.

    CAS  PubMed  Google Scholar 

  • Izumikawa T, Saigoh K, Shimizu J, Tsuji S, Kusunoki S, Kitagawa H. A chondroitin synthase-1 (ChSy-1) missense mutation in a patient with neuropathy impairs the elongation of chondroitin sulfate chains initiated by chondroitin N-acetylgalactosaminyltransferase-1. Biochim Biophys Acta. 2013;1830(10):4806–12.

    CAS  PubMed  Google Scholar 

  • Jaworski DM, Kelly GM, Hockfield S. The CNS-specific hyaluronan-binding protein BEHAB is expressed in ventricular zones coincident with gliogenesis. J Neurosci. 1995;15(2):1352–62.

    CAS  PubMed  Google Scholar 

  • Jen Y-HL, Musacchio M, Lander AD. Glypican-1 controls brain size through regulation of fibroblast growth factor signaling in early neurogenesis. Neural Dev. 2009;4:33.

    PubMed Central  PubMed  Google Scholar 

  • Johnson KG, Tenney AP, Ghose A, Duckworth AM, Higashi ME, Parfitt K, et al. The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron. 2006;49(4):517–31.

    CAS  PubMed  Google Scholar 

  • Kantor DB, Chivatakarn O, Peer KL, Oster SF, Inatani M, Hansen MJ, et al. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron. 2004;44(6):961–75.

    CAS  PubMed  Google Scholar 

  • Karumbaiah L, Anand S, Thazhath R, Zhong Y, McKeon RJ, Bellamkonda RV. Targeted downregulation of N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase significantly mitigates chondroitin sulfate proteoglycan-mediated inhibition. Glia. 2011;59(6):981–96.

    PubMed Central  PubMed  Google Scholar 

  • Kawashima H, Atarashi K, Hirose M, Hirose J, Yamada S, Sugahara K, et al. Oversulfated chondroitin/dermatan sulfates containing GlcAbeta1/IdoAalpha1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J Biol Chem. 2002;277(15):12921–30.

    CAS  PubMed  Google Scholar 

  • Kearns AE, Vertel BM, Schwartz NB. Topography of glycosylation and UDP-xylose production. J Biol Chem. 1993;268(15):11097–104.

    CAS  PubMed  Google Scholar 

  • Klaver DW, Wilce MC, Gasperini R, Freeman C, Juliano JP, Parish C, et al. Glycosaminoglycan-induced activation of the beta-secretase (BACE1) of Alzheimer’s disease. J Neurochem. 2010;112(6):1552–61.

    CAS  PubMed  Google Scholar 

  • Koike T, Izumikawa T, Tamura J, Kitagawa H. FAM20B is a kinase that phosphorylates xylose in the glycosaminoglycan-protein linkage region. Biochem J. 2009;421(2):157–62.

    CAS  PubMed  Google Scholar 

  • Kreuger J, Kjellen L. Heparan sulfate biosynthesis: regulation and variability. J Histochem Cytochem. 2012;60(12):898–907.

    PubMed Central  PubMed  Google Scholar 

  • Kuschert GS, Coulin F, Power CA, Proudfoot AE, Hubbard RE, Hoogewerf AJ, et al. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry. 1999;38(39):12959–68.

    CAS  PubMed  Google Scholar 

  • Lafont F, Rouget M, Triller A, Prochiantz A, Rousselet A. In vitro control of neuronal polarity by glycosaminoglycans. Development. 1992;114(1):17–29.

    CAS  PubMed  Google Scholar 

  • Lau E, Margolis RU. Inhibitors of slit protein interactions with the heparan sulphate proteoglycan glypican-1: potential agents for the treatment of spinal cord injury. Clin Exp Pharmacol Physiol. 2010;37(4):417–21.

    CAS  PubMed  Google Scholar 

  • Lee H, Leamey CA, Sawatari A. Rapid reversal of chondroitin sulfate proteoglycan associated staining in subcompartments of mouse neostriatum during the emergence of behaviour. PLoS One. 2008;3(8):e3020.

    PubMed Central  PubMed  Google Scholar 

  • Lehman TJ, Miller N, Norquist B, Underhill L, Keutzer J. Diagnosis of the mucopolysaccharidoses. Rheumatology. 2011;50 Suppl 5:v41–8.

    CAS  PubMed  Google Scholar 

  • Leveugle B, Ding W, Durkin JT, Mistretta S, Eisle J, Matic M, et al. Heparin promotes beta-secretase cleavage of the Alzheimer’s amyloid precursor protein. Neurochem Int. 1997;30(6):543–8.

    CAS  PubMed  Google Scholar 

  • Li JP, Gong F, Hagner-McWhirter A, Forsberg E, Abrink M, Kisilevsky R, et al. Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. J Biol Chem. 2003;278(31):28363–6.

    CAS  PubMed  Google Scholar 

  • Li Y, Laue K, Temtamy S, Aglan M, Kotan LD, Yigit G, et al. Temtamy preaxial brachydactyly syndrome is caused by loss-of-function mutations in chondroitin synthase 1, a potential target of BMP signaling. Am J Hum Genet. 2010;87(6):757–67.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin X. Functions of heparan sulfate proteoglycans in cell signaling during development. Development. 2004;131(24):6009–21.

    CAS  PubMed  Google Scholar 

  • Lin X, Wei G, Shi Z, Dryer L, Esko JD, Wells DE, et al. Disruption of gastrulation and heparan sulfate biosynthesis in EXT1- deficient mice. Dev Biol. 2000;224(2):299–311.

    CAS  PubMed  Google Scholar 

  • Lin R, Rosahl TW, Whiting PJ, Fawcett JW, Kwok JC. 6-Sulphated chondroitins have a positive influence on axonal regeneration. PLoS One. 2011;6(7):e21499.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Litwack ED, Ivins JK, Kumbasar A, Paine-Saunders S, Stipp CS, Lander AD. Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev Dyn. 1998;211(1):72–87.

    CAS  PubMed  Google Scholar 

  • Maeda N. Structural variation of chondroitin sulfate and its roles in the central nervous system. Cent Nerv Syst Agents Med Chem. 2010;10(1):22–31.

    CAS  PubMed  Google Scholar 

  • Maeda N, Fukazawa N, Hata T. The binding of chondroitin sulfate to pleiotrophin/heparin-binding growth-associated molecule is regulated by chain length and oversulfated structures. J Biol Chem. 2006;281(8):4894–902.

    CAS  PubMed  Google Scholar 

  • Maeda N, Ishii M, Nishimura K, Kamimura K. Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem Res. 2011;36(7):1228–40.

    CAS  PubMed  Google Scholar 

  • Malfait F, Syx D, Vlummens P, Symoens S, Nampoothiri S, Hermanns-Le T, et al. Musculocontractural Ehlers-Danlos Syndrome (former EDS type VIB) and adducted thumb clubfoot syndrome (ATCS) represent a single clinical entity caused by mutations in the dermatan-4-sulfotransferase 1 encoding CHST14 gene. Hum Mutat. 2010;31(11):1233–9.

    CAS  PubMed  Google Scholar 

  • Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, et al. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci. 2006;26(16):4406–14.

    CAS  PubMed  Google Scholar 

  • Matsumoto Y, Irie F, Inatani M, Tessier-Lavigne M, Yamaguchi Y. Netrin-1/DCC signaling in commissural axon guidance requires cell-autonomous expression of heparan sulfate. J Neurosci. 2007;27(16):4342–50.

    CAS  PubMed  Google Scholar 

  • McKillop WM, Dragan M, Schedl A, Brown A. Conditional Sox9 ablation reduces chondroitin sulfate proteoglycan levels and improves motor function following spinal cord injury. Glia. 2013;61(2):164–77.

    PubMed  Google Scholar 

  • McLaughlin D, Karlsson F, Tian N, Pratt T, Bullock SL, Wilson VA, et al. Specific modification of heparan sulphate is required for normal cerebral cortical development. Mech Dev. 2003;120(12):1481–8.

    CAS  PubMed  Google Scholar 

  • McRae PA, Rocco MM, Kelly G, Brumberg JC, Matthews RT. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci. 2007;27(20):5405–13.

    CAS  PubMed  Google Scholar 

  • Meyers EN, Lewandoski M, Martin GR. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet. 1998;18(2):136–41.

    CAS  PubMed  Google Scholar 

  • Mikami T, Kitagawa H. Biosynthesis and function of chondroitin sulfate. Biochim Biophys Acta. 2013;1830(10):4719–33.

    CAS  PubMed  Google Scholar 

  • Mikami T, Yasunaga D, Kitagawa H. Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J Biol Chem. 2009;284(7):4494–9.

    CAS  PubMed  Google Scholar 

  • Miyake N, Kosho T, Mizumoto S, Furuichi T, Hatamochi A, Nagashima Y, et al. Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome. Hum Mutat. 2010;31(8):966–74.

    CAS  PubMed  Google Scholar 

  • Mizumoto S, Mikami T, Yasunaga D, Kobayashi N, Yamauchi H, Miyake A, et al. Chondroitin 4-O-sulfotransferase-1 is required for somitic muscle development and motor axon guidance in zebrafish. Biochem J. 2009;419(2):387–99.

    CAS  PubMed  Google Scholar 

  • Mizumoto S, Fongmoon D, Sugahara K. Interaction of chondroitin sulfate and dermatan sulfate from various biological sources with heparin-binding growth factors and cytokines. Glycoconj J. 2013a;30(6):619–32.

    CAS  PubMed  Google Scholar 

  • Mizumoto S, Ikegawa S, Sugahara K. Human genetic disorders caused by mutations in genes encoding biosynthetic enzymes for sulfated glycosaminoglycans. J Biol Chem. 2013b;288(16):10953–61.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moon LD, Asher RA, Rhodes KE, Fawcett JW. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci. 2001;4(5):465–6.

    CAS  PubMed  Google Scholar 

  • Nandini CD, Itoh N, Sugahara K. Novel 70-kDa chondroitin sulfate/dermatan sulfate hybrid chains with a unique heterogeneous sulfation pattern from shark skin, which exhibit neuritogenic activity and binding activities for growth factors and neurotrophic factors. J Biol Chem. 2005;280(6):4058–69.

    CAS  PubMed  Google Scholar 

  • Nishimura K, Ishii M, Kuraoka M, Kamimura K, Maeda N. Opposing functions of chondroitin sulfate and heparan sulfate during early neuronal polarization. Neuroscience. 2010;169(4):1535–47.

    CAS  PubMed  Google Scholar 

  • Ohtake S, Ito Y, Fukuta M, Habuchi O. Human N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase cDNA is related to human B cell recombination activating gene-associated gene. J Biol Chem. 2001;276(47):43894–900.

    CAS  PubMed  Google Scholar 

  • Oohira A, Matsui F, Katoh-Semba R. Inhibitory effect of brain chondroitin sulphate proteoglycans on neurite outgrowth from PC12D cells. J Neurosci. 1991;11:822–7.

    CAS  PubMed  Google Scholar 

  • Orlando C, Ster J, Gerber U, Fawcett JW, Raineteau O. Perisynaptic chondroitin sulfate proteoglycans restrict structural plasticity in an integrin-dependent manner. J Neurosci. 2012;32(50):18009-17, 17a.

    Google Scholar 

  • Oyagi A, Hara H. Essential roles of heparin-binding epidermal growth factor-like growth factor in the brain. CNS Neurosci Ther. 2012;18(10):803–10.

    CAS  PubMed  Google Scholar 

  • Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science. 2002;298(5596):1248–51.

    CAS  PubMed  Google Scholar 

  • Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L. Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci U S A. 2006;103(22):8517–22.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pratt T, Conway CD, Tian NM, Price DJ, Mason JO. Heparan sulphation patterns generated by specific heparan sulfotransferase enzymes direct distinct aspects of retinal axon guidance at the optic chiasm. J Neurosci. 2006;26(26):6911–23.

    CAS  PubMed  Google Scholar 

  • Preston M, Sherman LS. Neural stem cell niches: roles for the hyaluronan-based extracellular matrix. Front Biosci. 2011;3:1165–79.

    Google Scholar 

  • Properzi F, Lin R, Kwok J, Naidu M, van Kuppevelt TH, Ten Dam GB, et al. Heparan sulphate proteoglycans in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur J Neurosci. 2008;27(3):593–604.

    PubMed  Google Scholar 

  • Rauch U, Kappler J. Chondroitin/Dermatan sulfates in the central nervous system: their structures and functions in health and disease. Adv Pharmacol. 2006;53:337–56.

    CAS  PubMed  Google Scholar 

  • Rauch U, Zhou XH, Roos G. Extracellular matrix alterations in brains lacking four of its components. Biochem Biophys Res Commun. 2005;328(2):608–17.

    CAS  PubMed  Google Scholar 

  • Raulo E, Tumova S, Pavlov I, Pekkanen M, Hienola A, Klankki E, et al. The two thrombospondin type I repeat domains of the heparin-binding growth-associated molecule bind to heparin/heparan sulfate and regulate neurite extension and plasticity in hippocampal neurons. J Biol Chem. 2005;280(50):41576–83.

    CAS  PubMed  Google Scholar 

  • Reizes O, Lincecum J, Wang Z, Goldberger O, Huang L, Kaksonen M, et al. Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell. 2001;106(1):105–16.

    CAS  PubMed  Google Scholar 

  • Romberg C, Yang S, Melani R, Andrews MR, Horner AE, Spillantini MG, et al. Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex. J Neurosci. 2013;33(16):7057–65.

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Saigoh K, Izumikawa T, Koike T, Shimizu J, Kitagawa H, Kusunoki S. Chondroitin beta-1,4-N-acetylgalactosaminyltransferase-1 missense mutations are associated with neuropathies. J Hum Genet. 2011;56(2):143–6.

    CAS  PubMed  Google Scholar 

  • Sakurai T, Friedlander DR, Grumet M. Expression of polypeptide variants of receptor-type protein tyrosine phosphatase beta: the secreted form, phosphacan, increases dramatically during embryonic development and modulates glial cell behavior in vitro. J Neurosci Res. 1996;43(6):694–706.

    CAS  PubMed  Google Scholar 

  • Saunders S, Paine-Saunders S, Lander AD. Expression of the cell surface proteoglycan glypican-5 is developmentally regulated in kidney, limb, and brain. Dev Biol. 1997;190(1):78–93.

    CAS  PubMed  Google Scholar 

  • Schmalfeldt M, Bandtlow CE, Dours-Zimmermann MT, Winterhalter KH, Zimmermann DR. Brain derived versican V2 is a potent inhibitor of axonal growth. J Cell Sci. 2000;113(Pt 5):807–16.

    CAS  PubMed  Google Scholar 

  • Schwartz NB. Biosynthesis and regulation of expression of proteoglycans. Front Biosci. 2000;5:D649–55.

    CAS  PubMed  Google Scholar 

  • Schwartz NB. PAPS and sulfoconjugation. In: Coughtrie MW, Pacifici GM, editors. Human cytosolic sulfotransferases. London: Taylor & Francis; 2005. p. 43–60.

    Google Scholar 

  • Schwartz NB. Special pathways and glycoconjugates. In: Devlin TM, editor. Textbook of biochemistry. 7th ed. New York: Wiley Liss; 2010. p. 647–73.

    Google Scholar 

  • Schwartz, Nancy B. Proteoglycans. In: Encyclopedia of Life Sciences. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000623.pub2]; 2009.

  • Shah A, Lodge DJ. A loss of hippocampal perineuronal nets produces deficits in dopamine system function: relevance to the positive symptoms of schizophrenia. Transl Psychiatry. 2013;3:e215.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, et al. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science. 2009;326(5952):592–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shi J, Potash JB, Knowles JA, Weissman MM, Coryell W, Scheftner WA, et al. Genome-wide association study of recurrent early-onset major depressive disorder. Mol Psychiatry. 2011;16(2):193–201.

    CAS  PubMed  Google Scholar 

  • Shimazaki Y, Nagata I, Ishii M, Tanaka M, Marunouchi T, Hata T, et al. Developmental change and function of chondroitin sulfate deposited around cerebellar Purkinje cells. J Neurosci Res. 2005;82(2):172–83.

    CAS  PubMed  Google Scholar 

  • Shipp EL, Hsieh-Wilson LC. Profiling the sulfation specificities of glycosaminoglycan interactions with growth factors and chemotactic proteins using microarrays. Chem Biol. 2007;14(2):195–208.

    CAS  PubMed  Google Scholar 

  • Shriver Z, Capila I, Venkataraman G, Sasisekharan R. Heparin and heparan sulfate: analyzing structure and microheterogeneity. Handb Exp Pharmacol. 2012;207:159–76.

    CAS  PubMed  Google Scholar 

  • Silbert JE, Sugumaran G. Biosynthesis of chondroitin/dermatan sulfate. IUBMB Life. 2002;54(4):177–86.

    CAS  PubMed  Google Scholar 

  • Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci. 2004;5(2):146–56.

    CAS  PubMed  Google Scholar 

  • Sirko S, von Holst A, Wizenmann A, Gotz M, Faissner A. Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development. 2007;134(15):2727–38.

    CAS  PubMed  Google Scholar 

  • Sirko S, Akita K, Von Holst A, Faissner A. Structural and functional analysis of chondroitin sulfate proteoglycans in the neural stem cell niche. Methods Enzymol. 2010a;479:37–71.

    CAS  PubMed  Google Scholar 

  • Sirko S, von Holst A, Weber A, Wizenmann A, Theocharidis U, Gotz M, et al. Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells. 2010b;28(4):775–87.

    CAS  PubMed  Google Scholar 

  • Snyder SE, Li J, Schauwecker PE, McNeill TH, Salton SR. Comparison of RPTP zeta/beta, phosphacan, and trkB mRNA expression in the developing and adult rat nervous system and induction of RPTP zeta/beta and phosphacan mRNA following brain injury. Brain Res Mol Brain Res. 1996;40(1):79–96.

    CAS  PubMed  Google Scholar 

  • Struve J, Maher PC, Li YQ, Kinney S, Fehlings MG, Kuntz CT, et al. Disruption of the hyaluronan-based extracellular matrix in spinal cord promotes astrocyte proliferation. Glia. 2005;52(1):16–24.

    PubMed  Google Scholar 

  • Sugahara K, Kitagawa H. Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr Opin Struct Biol. 2000;10(5):518–27.

    CAS  PubMed  Google Scholar 

  • Sweeney MD, Yu Y, Leary JA. Effects of sulfate position on heparin octasaccharide binding to CCL2 examined by tandem mass spectrometry. J Am Soc Mass Spectrom. 2006;17(8):1114–9.

    CAS  PubMed  Google Scholar 

  • Takahashi N, Sakurai T, Bozdagi-Gunal O, Dorr NP, Moy J, Krug L, et al. Increased expression of receptor phosphotyrosine phosphatase-beta/zeta is associated with molecular, cellular, behavioral and cognitive schizophrenia phenotypes. Transl Psychiatry. 2011;1:e8.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tham M, Ramasamy S, Gan HT, Ramachandran A, Poonepalli A, Yu YH, et al. CSPG is a secreted factor that stimulates neural stem cell survival possibly by enhanced EGFR signaling. PLoS One. 2010;5(12):e15341.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tian J, Ling L, Shboul M, Lee H, O’Connor B, Merriman B, et al. Loss of CHSY1, a secreted FRINGE enzyme, causes syndromic brachydactyly in humans via increased NOTCH signaling. Am J Hum Genet. 2010;87(6):768–78.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tom VJ, Kadakia R, Santi L, Houle JD. Administration of chondroitinase ABC rostral or caudal to a spinal cord injury site promotes anatomical but not functional plasticity. J Neurotrauma. 2009;26(12):2323–33.

    PubMed Central  PubMed  Google Scholar 

  • Tone Y, Pedersen LC, Yamamoto T, Izumikawa T, Kitagawa H, Nishihara J, et al. 2-o-phosphorylation of xylose and 6-o-sulfation of galactose in the protein linkage region of glycosaminoglycans influence the glucuronyltransferase-I activity involved in the linkage region synthesis. J Biol Chem. 2008;283(24):16801–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Uchimura K, Kadomatsu K, Nishimura H, Muramatsu H, Nakamura E, Kurosawa N, et al. Functional analysis of the chondroitin 6-sulfotransferase gene in relation to lymphocyte subpopulations, brain development, and oversulfated chondroitin sulfates. J Biol Chem. 2002;277(2):1443–50.

    CAS  PubMed  Google Scholar 

  • Ughrin YM, Chen ZJ, Levine JM. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci. 2003;23(1):175–86.

    CAS  PubMed  Google Scholar 

  • Uyama T, Kitagawa K, Sugahara H. Biosynthesis of glycosaminoglycans and proteoglycans. In: Kamerling JP, editor. Comprehensive glycoscience, vol. 3. Amsterdam: Elsevier; 2007. p. 79–104.

    Google Scholar 

  • van Horssen J, Wesseling P, van den Heuvel LP, de Waal RM, Verbeek MM. Heparan sulphate proteoglycans in Alzheimer’s disease and amyloid-related disorders. Lancet Neurol. 2003;2(8):482–92.

    PubMed  Google Scholar 

  • Vertel BM, Walters LM, Flay N, Kearns AE, Schwartz NB. Xylosylation is an endoplasmic reticulum to Golgi event. J Biol Chem. 1993;268(15):11105–12.

    CAS  PubMed  Google Scholar 

  • Vo T, Carulli D, Ehlert EM, Kwok JC, Dick G, Mecollari V, et al. The chemorepulsive axon guidance protein semaphorin3A is a constituent of perineuronal nets in the adult rodent brain. Mol Cell Neurosci. 2013;56C:186–200.

    Google Scholar 

  • Wang D, Fawcett J. The perineuronal net and the control of CNS plasticity. Cell Tissue Res. 2012;349(1):147–60.

    PubMed  Google Scholar 

  • Wang K, Zhang H, Ma D, Bucan M, Glessner JT, Abrahams BS, et al. Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature. 2009;459(7246):528–33.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang Q, Yang L, Alexander C, Temple S. The niche factor syndecan-1 regulates the maintenance and proliferation of neural progenitor cells during mammalian cortical development. PLoS One. 2012;7(8):e42883.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wegrzyn G, Jakobkiewicz-Banecka J, Narajczyk M, Wisniewski A, Piotrowska E, Gabig-Ciminska M, et al. Why are behaviors of children suffering from various neuronopathic types of mucopolysaccharidoses different? Med Hypotheses. 2010;75(6):605–9.

    CAS  PubMed  Google Scholar 

  • Yamaguchi Y. Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci. 2000;57(2):276–89.

    CAS  PubMed  Google Scholar 

  • Yamaguchi Y, Inatani M, Matsumoto Y, Ogawa J, Irie F. Roles of heparan sulfate in mammalian brain development current views based on the findings from Ext1 conditional knockout studies. Prog Mol Biol Transl Sci. 2010;93:133–52.

    CAS  PubMed  Google Scholar 

  • Ye Q, Miao QL. Experience-dependent development of perineuronal nets and chondroitin sulfate proteoglycan receptors in mouse visual cortex. Matrix Biol. 2013;32(6):352–63.

    CAS  PubMed  Google Scholar 

  • Zafeiriou DI, Batzios SP. Brain and spinal MR imaging findings in mucopolysaccharidoses: a review. AJNR Am J Neuroradiol. 2013;34(1):5–13.

    CAS  PubMed  Google Scholar 

  • Zhang H, Muramatsu T, Murase A, Yuasa S, Uchimura K, Kadomatsu K. N-Acetylglucosamine 6-O-sulfotransferase-1 is required for brain keratan sulfate biosynthesis and glial scar formation after brain injury. Glycobiology. 2006a;16(8):702–10.

    CAS  PubMed  Google Scholar 

  • Zhang H, Uchimura K, Kadomatsu K. Brain keratan sulfate and glial scar formation. Ann N Y Acad Sci. 2006b;1086:81–90.

    CAS  PubMed  Google Scholar 

  • Zhao RR, Andrews MR, Wang D, Warren P, Gullo M, Schnell L, et al. Combination treatment with anti-Nogo-A and chondroitinase ABC is more effective than single treatments at enhancing functional recovery after spinal cord injury. The European journal of neuroscience. 2013;38(6):2946–61.

    PubMed  Google Scholar 

  • Zou P, Zou K, Muramatsu H, Ichihara-Tanaka K, Habuchi O, Ohtake S, et al. Glycosaminoglycan structures required for strong binding to midkine, a heparin-binding growth factor. Glycobiology. 2003;13(1):35–42.

    CAS  PubMed  Google Scholar 

  • Zuo J, Neubauer D, Graham J, Krekoski CA, Ferguson TA, Muir D. Regeneration of axons after nerve transection repair is enhanced by degradation of chondroitin sulfate proteoglycan. Exp Neurol. 2002;176(1):221–8.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This work was supported by grants from the National Institute of Child Health and Human Disorders (P01-HD 09402, P30-HD0054275, R03 HD00354235).

Conflict of Interest The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Pediatrics, University of Chicago, Chicago, IL, 60637, USA

    Nancy B. Schwartz & Miriam S. Domowicz

  2. Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL, 60637, USA

    Nancy B. Schwartz

Authors
  1. Nancy B. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miriam S. Domowicz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nancy B. Schwartz .

Editor information

Editors and Affiliations

  1. Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Georgia Regents University, Augusta, Georgia, USA

    Robert K. Yu

  2. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, College of Medicine, Hershey, Pennsylvania, USA

    Cara-Lynne Schengrund

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Schwartz, N.B., Domowicz, M.S. (2014). Chemistry and Function of Glycosaminoglycans in the Nervous System. 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_5

Download citation

Publish with us

Policies and ethics

Search

Navigation