Home LiteratureArticle Details
PMID: 16162928 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Versican in the developing brain: lamina-specific expression in interneuronal subsets and role in presynaptic maturation.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 25 ·No. 37 ·2005-09-14 ·Pages 8457-67

Yamagata M, Sanes JR

Abstract

Chondroitin sulfate proteoglycans (CSPGs) of the extracellular matrix help stabilize synaptic connections in the postnatal brain and impede regeneration after injury. Here, we show that a CSPG of the lectican family, versican, also promotes presynaptic maturation in the developing brain. In the embryonic chick optic tectum, versican is expressed selectively by subsets of interneurons confined to the retinorecipient laminae, in which retinal axons arborize and form synapses. It is a major receptor for the Vicia villosa B4 lectin (VVA), shown previously to inhibit invasion of the retinorecipient lamina by retinal axons (Inoue and Sanes, 1997). In vitro, versican promotes enlargement of presynaptic varicosities in retinal axons. Depletion of versican in ovo, by RNA interference, results in retinal arbors with smaller than normal varicosities. We propose that versican provides a lamina-specific cue for presynaptic maturation and discuss the related but distinct effects of versican depletion and VVA blockade.

MeSH Terms
Animals Axons/physiology Cells, Cultured Chondroitin Sulfate Proteoglycans/physiology Hippocampus/embryology,physiology Lectins, C-Type/physiology Neurons/physiology Optic Nerve/embryology,physiology Proteoglycans Superior Colliculi/embryology,physiology Synapses/physiology Versicans
Chemicals
Chondroitin Sulfate Proteoglycans Lectins, C-Type Proteoglycans Versicans
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Yamagata Masahito
Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Sanes Joshua R
References (77)
77 references, click to expand
  1. Fine structure of the optic fibre termination layers in the pigeon optic tectum: a Golgi and electron microscope study.
    Neuroscience. 1976;1(2):93-105 PMID: 1004710
  2. Distinct structures and functions of related pre- and postsynaptic carbohydrates at the mammalian neuromuscular junction.
    Mol Cell Neurosci. 1999 Feb;13(2):105-18 PMID: 10192769
  3. Efficient targeting of gene expression in chick embryos by microelectroporation.
    Dev Growth Differ. 1999 Jun;41(3):335-44 PMID: 10400395
  4. Laminar redistribution of a glial subtype in the chick optic tectum.
    Brain Res Dev Brain Res. 1999 Jun 2;115(2):103-9 PMID: 10407128
  5. Immunohistochemical evidence for the brevican-tenascin-R interaction: colocalization in perineuronal nets suggests a physiological role for the interaction in the adult rat brain.
    J Comp Neurol. 1999 Jul 26;410(2):256-64 PMID: 10414531
  6. Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans.
    J Neurosci. 1999 Oct 15;19(20):8979-89 PMID: 10516316
  7. Brain derived versican V2 is a potent inhibitor of axonal growth.
    J Cell Sci. 2000 Mar;113 ( Pt 5):807-16 PMID: 10671370
  8. Direct connections between dendritic terminals of tectal ganglion cells and glutamate-positive terminals of presumed optic fibres in layers 4-5 of the optic tectum of Gallus domesticus. A light- and electron microscopic study.
    Neurobiology (Bp). 1999;7(1):45-67 PMID: 10746250
  9. Lecticans: organizers of the brain extracellular matrix.
    Cell Mol Life Sci. 2000 Feb;57(2):276-89 PMID: 10766023
  10. Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan.
    J Cell Biol. 2000 Jun 12;149(6):1275-88 PMID: 10851024
  11. Biosynthesis and regulation of expression of proteoglycans.
    Front Biosci. 2000 Jul 01;5:D649-55 PMID: 10877997
  12. Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44.
    J Biol Chem. 2000 Nov 10;275(45):35448-56 PMID: 10950950
  13. Proteoglycans in the developing brain: new conceptual insights for old proteins.
    Physiol Rev. 2000 Oct;80(4):1267-90 PMID: 11015614
  14. The proteoglycans aggrecan and Versican form networks with fibulin-2 through their lectin domain binding.
    J Biol Chem. 2001 Jan 12;276(2):1253-61 PMID: 11038354
  15. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC.
    Nat Neurosci. 2001 May;4(5):465-6 PMID: 11319553
  16. Differential Vicia villosa agglutinin reactivity identifies three distinct dystroglycan complexes in skeletal muscle.
    J Biol Chem. 2001 Sep 14;276(37):35078-86 PMID: 11459841
  17. An electron microscope study of the retino-receptive layers of the pigeon optic tectum.
    J Comp Neurol. 1975 Aug 15;162(4):447-65 PMID: 1150929
  18. beta 1-Integrin-mediated glioma cell adhesion and free radical-induced apoptosis are regulated by binding to a C-terminal domain of PG-M/versican.
    J Biol Chem. 2002 Apr 5;277(14):12294-301 PMID: 11805102
  19. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells.
    J Neurosci. 2002 Mar 15;22(6):2225-36 PMID: 11896162
  20. A system for stable expression of short interfering RNAs in mammalian cells.
    Science. 2002 Apr 19;296(5567):550-3 PMID: 11910072
  21. Chondroitinase ABC promotes functional recovery after spinal cord injury.
    Nature. 2002 Apr 11;416(6881):636-40 PMID: 11948352
  22. Molecular cloning and characterization of chick sialoprotein associated with cones and rods, a developmentally regulated glycoprotein of interphotoreceptor matrix.
    J Biol Chem. 2002 Jul 12;277(28):25592-600 PMID: 11991949
  23. Annexin 6 is a putative cell surface receptor for chondroitin sulfate chains.
    J Cell Sci. 2002 Aug 15;115(Pt 16):3309-18 PMID: 12140262
  24. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets.
    J Neurosci. 2002 Sep 1;22(17):7536-47 PMID: 12196577
  25. Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina.
    Cell. 2002 Sep 6;110(5):649-60 PMID: 12230981
  26. Versican: a versatile extracellular matrix proteoglycan in cell biology.
    Curr Opin Cell Biol. 2002 Oct;14(5):617-23 PMID: 12231358
  27. Reactivation of ocular dominance plasticity in the adult visual cortex.
    Science. 2002 Nov 8;298(5596):1248-51 PMID: 12424383
  28. Spotted substrates for focal presentation of proteins to cells.
    Biotechniques. 2002 Nov;33(5):1018-20, 1022, 1024 PMID: 12449378
  29. Localization of aggrecan and versican in the developing rat central nervous system.
    Dev Dyn. 2003 May;227(1):143-9 PMID: 12701107
  30. MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb.
    Nat Cell Biol. 2003 Jun;5(6):513-9 PMID: 12766772
  31. Extracellular matrix molecules and synaptic plasticity.
    Nat Rev Neurosci. 2003 Jun;4(6):456-68 PMID: 12778118
  32. Distinct interaction of versican/PG-M with hyaluronan and link protein.
    J Biol Chem. 2003 Oct 17;278(42):41205-12 PMID: 12888576
  33. Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats.
    J Neurosci. 2003 Aug 6;23(18):7034-44 PMID: 12904464
  34. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS?
    J Anat. 2004 Jan;204(1):33-48 PMID: 14690476
  35. The ramifications and terminals of optic fibres in layers 2 and 3 of the avian optic tectum: a golgi and light and electron microscopic anterograde tracer study.
    Cells Tissues Organs. 2003;175(4):202-22 PMID: 14707401
  36. Regeneration beyond the glial scar.
    Nat Rev Neurosci. 2004 Feb;5(2):146-56 PMID: 14735117
  37. Versican V1 isoform induces neuronal differentiation and promotes neurite outgrowth.
    Mol Biol Cell. 2004 May;15(5):2093-104 PMID: 14978219
  38. Developmental changes of aggrecan, versican and neurocan in the retina and optic nerve.
    Exp Eye Res. 2004 Sep;79(3):351-6 PMID: 15336497
  39. Versican V2 and the central inhibitory domain of Nogo-A inhibit neurite growth via p75NTR/NgR-independent pathways that converge at RhoA.
    Mol Cell Neurosci. 2004 Oct;27(2):163-74 PMID: 15485772
  40. Extracellular matrix and visual cortical plasticity: freeing the synapse.
    Neuron. 2004 Dec 16;44(6):905-8 PMID: 15603733
  41. Defining nucleic acid-binding properties of avian retrovirus integrase by deletion analysis.
    J Virol. 1991 Mar;65(3):1160-7 PMID: 1847445
  42. Synaptic localization and neural regulation of an N-acetylgalactosaminyl transferase in skeletal muscle.
    J Neurosci. 1990 Jan;10(1):346-50 PMID: 2105381
  43. Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain.
    Cold Spring Harb Symp Quant Biol. 1990;55:505-14 PMID: 2132834
  44. Comparison of the carbohydrate-binding specificities of seven N-acetyl-D-galactosamine-recognizing lectins.
    Eur J Biochem. 1990 Jul 31;191(2):461-6 PMID: 2384093
  45. The role of cell adhesion molecules in neurite outgrowth on Müller cells.
    Dev Biol. 1990 Mar;138(1):82-93 PMID: 2407579
  46. Regulation of cell-substrate adhesion by proteoglycans immobilized on extracellular substrates.
    J Biol Chem. 1989 May 15;264(14):8012-8 PMID: 2470739
  47. Production and characterization of monoclonal antibodies directed against connective tissue proteoglycans.
    Fed Proc. 1985 Feb;44(2):386-93 PMID: 2578417
  48. Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors.
    J Virol. 1987 Oct;61(10):3004-12 PMID: 3041020
  49. A synapse-specific carbohydrate at the neuromuscular junction: association with both acetylcholinesterase and a glycolipid.
    J Neurosci. 1988 Mar;8(3):932-44 PMID: 3346730
  50. Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro.
    Development. 1987 Dec;101(4):685-96 PMID: 3503693
  51. A large chondroitin sulfate proteoglycan (PG-M) synthesized before chondrogenesis in the limb bud of chick embryo.
    J Biol Chem. 1986 Oct 15;261(29):13517-25 PMID: 3759975
  52. Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin.
    J Biol Chem. 1986 Oct 15;261(29):13526-35 PMID: 3759976
  53. Induction of glutamine synthetase in embryonic neural retina: its suppression by the gliatoxic agent alpha-aminoadipic acid.
    Brain Res. 1981 Jan;227(1):103-19 PMID: 6110468
  54. Oriented axon outgrowth from avian embryonic retinae in culture.
    Dev Biol. 1983 Jan;95(1):56-64 PMID: 6825932
  55. Disappearance of the Vicia villosa-positivity from the perineuronal net containing chondroitin proteoglycan after chondroitinase digestion.
    Brain Res. 1995 Mar 6;673(2):344-8 PMID: 7606451
  56. Versican, a hyaluronate-binding proteoglycan of embryonal precartilaginous mesenchyma, is mainly expressed postnatally in rat brain.
    J Neurosci Res. 1993 Jan;34(1):97-106 PMID: 7678658
  57. Role for a synapse-specific carbohydrate in agrin-induced clustering of acetylcholine receptors.
    Neuron. 1995 Apr;14(4):743-54 PMID: 7718237
  58. Lamina-specific expression of adhesion molecules in developing chick optic tectum.
    J Neurosci. 1995 Jun;15(6):4556-71 PMID: 7790923
  59. Lamina-specific cues guide outgrowth and arborization of retinal axons in the optic tectum.
    Development. 1995 Jan;121(1):189-200 PMID: 7867499
  60. Isolation and characterization of proteoglycans.
    Methods Enzymol. 1994;230:390-417 PMID: 8139509
  61. Selective distributions of proteoglycans and their ligands in pericellular matrix of cultured fibroblasts. Implications for their roles in cell-substratum adhesion.
    J Cell Sci. 1993 Sep;106 ( Pt 1):55-65 PMID: 8270643
  62. Developmentally regulated and spatially restricted antigens of radial glial cells.
    Dev Dyn. 1993 Aug;197(4):307-18 PMID: 8292827
  63. cDNA cloning of PG-M, a large chondroitin sulfate proteoglycan expressed during chondrogenesis in chick limb buds. Alternative spliced multiforms of PG-M and their relationships to versican.
    J Biol Chem. 1993 Jul 5;268(19):14461-9 PMID: 8314802
  64. Tissue variation of two large chondroitin sulfate proteoglycans (PG-M/versican and PG-H/aggrecan) in chick embryos.
    Anat Embryol (Berl). 1993 May;187(5):433-44 PMID: 8342790
  65. Nervous tissue proteoglycans.
    Experientia. 1993 May 15;49(5):429-46 PMID: 8500598
  66. Target-independent diversification and target-specific projection of chemically defined retinal ganglion cell subsets.
    Development. 1995 Nov;121(11):3763-76 PMID: 8582286
  67. High efficiency gene transfer into the embryonic chicken CNS using B-subgroup retroviruses.
    Dev Dyn. 1996 May;206(1):112-20 PMID: 9019242
  68. Alternative splicing of the unique "PLUS" domain of chicken PG-M/versican is developmentally regulated.
    J Biol Chem. 1997 Apr 4;272(14):9325-31 PMID: 9083069
  69. Lamina-specific connectivity in the brain: regulation by N-cadherin, neurotrophins, and glycoconjugates.
    Science. 1997 May 30;276(5317):1428-31 PMID: 9162013
  70. The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety.
    Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10116-21 PMID: 9294172
  71. Labeling of pyramidal and nonpyramidal neurons with lectin Vicia villosa during postnatal development of the guinea pig.
    J Comp Neurol. 1997 Dec 22;389(3):453-68 PMID: 9414006
  72. Occurrence of a N-terminal proteolytic fragment of neurocan, not a C-terminal half, in a perineuronal net in the adult rat cerebrum.
    Brain Res. 1998 Apr 20;790(1-2):45-51 PMID: 9593817
  73. Versican V2 is a major extracellular matrix component of the mature bovine brain.
    J Biol Chem. 1998 Jun 19;273(25):15758-64 PMID: 9624174
  74. Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican.
    Biochem Biophys Res Commun. 1998 Jun 18;247(2):207-12 PMID: 9642104
  75. The G3 domain of versican enhances cell proliferation via epidermial growth factor-like motifs.
    J Biol Chem. 1998 Aug 14;273(33):21342-51 PMID: 9694895
  76. Expression of multiple cadherins and catenins in the chick optic tectum.
    Mol Cell Neurosci. 1998 Nov;12(4-5):240-55 PMID: 9828089
  77. Perineuronal nets: past and present.
    Trends Neurosci. 1998 Dec;21(12):510-5 PMID: 9881847
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
DOI
10.1523/JNEUROSCI.1976-05.2005
Published
2005-09-14
Pages
8457-67
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6725682
Subset
IM
Corrections
CommentIn
PMID: 16436591
External Links
PubMed source DOI: 10.1523/JNEUROSCI.1976-05.2005 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2