Home LiteratureArticle Details
PMID: 7513709 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth.

The Journal of cell biology ·Vol. 125 ·No. 3 ·1994-05-00 ·Pages 669-80

Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M

Abstract

We have previously shown that aggregation of microbeads coated with N-CAM and Ng-CAM is inhibited by incubation with soluble neurocan, a chondroitin sulfate proteoglycan of brain, suggesting that neurocan binds to these cell adhesion molecules (Grumet, M., A. Flaccus, and R. U. Margolis. 1993. J. Cell Biol. 120:815). To investigate these interactions more directly, we have tested binding of soluble 125I-neurocan to microwells coated with different glycoproteins. Neurocan bound at high levels to Ng-CAM and N-CAM, but little or no binding was detected to myelin-associated glycoprotein, EGF receptor, fibronectin, laminin, and collagen IV. The binding to Ng-CAM and N-CAM was saturable and in each case Scatchard plots indicated a high affinity binding site with a dissociation constant of approximately 1 nM. Binding was significantly reduced after treatment of neurocan with chondroitinase, and free chondroitin sulfate inhibited binding of neurocan to Ng-CAM and N-CAM. These results indicate a role for chondroitin sulfate in this process, although the core glycoprotein also has binding activity. The COOH-terminal half of neurocan was shown to have binding properties essentially identical to those of the full-length proteoglycan. To study the potential biological functions of neurocan, its effects on neuronal adhesion and neurite growth were analyzed. When neurons were incubated on dishes coated with different combinations of neurocan and Ng-CAM, neuronal adhesion and neurite extension were inhibited. Experiments using anti-Ng-CAM antibodies as a substrate also indicate that neurocan has a direct inhibitory effect on neuronal adhesion and neurite growth. Immunoperoxidase staining of tissue sections showed that neurocan, Ng-CAM, and N-CAM are all present at highest concentration in the molecular layer and fiber tracts of developing cerebellum. The overlapping localization in vivo, the molecular binding studies, and the striking effects on neuronal adhesion and neurite growth support the view that neurocan may modulate neuronal adhesion and neurite growth during development by binding to neural cell adhesion molecules.

MeSH Terms
Aggrecans Animals Brain/embryology,metabolism Cell Adhesion/drug effects Cell Adhesion Molecules, Neuronal/metabolism Cell Differentiation/drug effects Chick Embryo Chondroitin Sulfate Proteoglycans/metabolism Collagen/metabolism Extracellular Matrix Proteins/metabolism Lectins, C-Type Nerve Tissue Proteins/metabolism Neurites/ultrastructure Neurocan Neurons/metabolism Protein Binding Proteoglycans/metabolism Rats Tenascin
Chemicals
Acan protein, rat Aggrecans Cell Adhesion Molecules, Neuronal Chondroitin Sulfate Proteoglycans Extracellular Matrix Proteins Lectins, C-Type Nerve Tissue Proteins Neurocan Proteoglycans Tenascin NCAN protein, human Collagen
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Friedlander D R
Department of Pharmacology, New York University Medical Center, New York 10016.
Milev P
Karthikeyan L
Margolis R K
Margolis R U
Grumet M
References (54)
54 references, click to expand
  1. Two antigenically related neuronal cell adhesion molecules of different specificities mediate neuron-neuron and neuron-glia adhesion.
    Proc Natl Acad Sci U S A. 1984 Jan;81(1):267-71 PMID: 6364137
  2. Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but are anti-adhesive.
    J Cell Biol. 1991 Nov;115(3):779-94 PMID: 1918163
  3. Molecular cloning of NILE glycoprotein and evidence for its continued expression in mature rat CNS.
    J Neurosci Res. 1991 Nov;30(3):567-81 PMID: 1800773
  4. Cell adhesion molecules: implications for a molecular histology.
    Annu Rev Biochem. 1991;60:155-90 PMID: 1883195
  5. Putative inhibitory extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesions.
    Dev Biol. 1993 Mar;156(1):34-48 PMID: 7680631
  6. Characteristics of proteoglycans extracted from the Swarm rat chondrosarcoma with associative solvents.
    J Biol Chem. 1979 Feb 25;254(4):1375-80 PMID: 762133
  7. Comparison of two cell surface molecules involved in neural cell adhesion.
    EMBO J. 1984 Feb;3(2):461-5 PMID: 6201360
  8. J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth.
    J Cell Biol. 1991 Jun;113(5):1159-71 PMID: 1710226
  9. Topology of cell adhesion molecules.
    Proc Natl Acad Sci U S A. 1989 Feb;86(3):1088-92 PMID: 2915974
  10. Functional characterization of chondroitin sulfate proteoglycans of brain: interactions with neurons and neural cell adhesion molecules.
    J Cell Biol. 1993 Feb;120(3):815-24 PMID: 8425902
  11. Isolation and characterization of developmentally regulated chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies.
    J Biol Chem. 1991 Aug 5;266(22):14785-801 PMID: 1907283
  12. Two immunologically and developmentally distinct chondroitin sulfate proteolglycans in embryonic chick brain.
    J Biol Chem. 1992 Jun 15;267(17):12149-61 PMID: 1601881
  13. Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain.
    J Biol Chem. 1992 Sep 25;267(27):19536-47 PMID: 1326557
  14. Expression of adhesion molecules and the establishment of boundaries during embryonic and neural development.
    Exp Neurol. 1990 Jul;109(1):6-18 PMID: 2192909
  15. Core proteins of soluble chondroitin sulfate proteoglycans purified from the rat brain block the cell cycle of PC12D cells.
    J Cell Physiol. 1993 Jul;156(1):17-23 PMID: 8314855
  16. Neurite outgrowth on a step gradient of chondroitin sulfate proteoglycan (CS-PG).
    J Neurobiol. 1992 Apr;23(3):322-36 PMID: 1624935
  17. Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in the development of an axon barrier.
    Dev Biol. 1990 Apr;138(2):359-76 PMID: 1690673
  18. Selective expression of the 180-kD component of the neural cell adhesion molecule N-CAM during development.
    J Cell Biol. 1985 Nov;101(5 Pt 1):1921-9 PMID: 3902857
  19. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1.
    Nature. 1984 Sep 13-19;311(5982):153-5 PMID: 6206400
  20. Polypeptide components and binding functions of neuron-glia cell adhesion molecules.
    Proc Natl Acad Sci U S A. 1984 Dec;81(24):7989-93 PMID: 6393132
  21. Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin.
    Nature. 1988 Aug 25;334(6184):701-3 PMID: 3412448
  22. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro.
    Exp Neurol. 1990 Jul;109(1):111-30 PMID: 2141574
  23. Neuronal cell adhesion molecule contactin/F11 binds to tenascin via its immunoglobulin-like domains.
    J Cell Biol. 1992 Oct;119(1):203-13 PMID: 1382076
  24. Inhibitors of neurite growth.
    Annu Rev Neurosci. 1993;16:565-95 PMID: 7681638
  25. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  26. O-linked sugar chain of human granulocyte colony-stimulating factor protects it against polymerization and denaturation allowing it to retain its biological activity.
    J Biol Chem. 1990 Jul 15;265(20):11432-5 PMID: 1694845
  27. Effects of beta-xylosides on proteoglycan biosynthesis and morphology of PC12 pheochromocytoma cells and primary cultures of rat cerebellum.
    J Cell Sci. 1991 Jun;99 ( Pt 2):237-46 PMID: 1909336
  28. The role of proteoglycans in cell adhesion, migration and proliferation.
    Curr Opin Cell Biol. 1992 Oct;4(5):793-801 PMID: 1419056
  29. The epidermal growth factor receptor as a multifunctional allosteric protein.
    Biochemistry. 1988 May 3;27(9):3119-23 PMID: 3291943
  30. Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule.
    Proc Natl Acad Sci U S A. 1983 Sep;80(18):5762-6 PMID: 6577452
  31. Spatial and temporal changes in the distribution of proteoglycans during avian neural crest development.
    Development. 1991 Feb;111(2):583-99 PMID: 1893876
  32. Distinct calcium-independent and calcium-dependent adhesion systems of chicken embryo cells.
    Proc Natl Acad Sci U S A. 1981 Jan;78(1):387-91 PMID: 6165990
  33. Nervous tissue proteoglycans.
    Experientia. 1993 May 15;49(5):429-46 PMID: 8500598
  34. Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons.
    Cell. 1992 Jan 24;68(2):303-22 PMID: 1733501
  35. Ligand: a versatile computerized approach for characterization of ligand-binding systems.
    Anal Biochem. 1980 Sep 1;107(1):220-39 PMID: 6254391
  36. Neural cell adhesion molecules influence second messenger systems.
    Neuron. 1989 Jul;3(1):13-20 PMID: 2559759
  37. Functional mapping of cytotactin: proteolytic fragments active in cell-substrate adhesion.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2329-40 PMID: 2461950
  38. Structure of the chicken neuron-glia cell adhesion molecule, Ng-CAM: origin of the polypeptides and relation to the Ig superfamily.
    J Cell Biol. 1991 Mar;112(5):1017-29 PMID: 1705558
  39. Chondroitin sulfate as a regulator of neuronal patterning in the retina.
    Science. 1992 Feb 7;255(5045):733-6 PMID: 1738848
  40. Cell adhesion molecules, second messengers and axonal growth.
    Curr Opin Neurobiol. 1992 Oct;2(5):595-601 PMID: 1422115
  41. Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase.
    Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2512-6 PMID: 7511813
  42. Proteoglycans in cell regulation.
    J Biol Chem. 1989 Aug 15;264(23):13369-72 PMID: 2668264
  43. Structure, expression, and function of Ng-CAM, a member of the immunoglobulin superfamily involved in neuron-neuron and neuron-glia adhesion.
    J Neurosci Res. 1992 Jan;31(1):1-13 PMID: 1377280
  44. Extracellular matrix molecules and their receptors: functions in neural development.
    Annu Rev Neurosci. 1991;14:531-70 PMID: 1851608
  45. Fractionation and properties of a chondroitin sulfate proteoglycan and the soluble glycoproteins of brain.
    J Biol Chem. 1981 Oct 25;256(20):10529-37 PMID: 6793583
  46. Regulation of axonal growth in the vertebrate nervous system by interactions between glycoproteins belonging to two subgroups of the immunoglobulin superfamily.
    J Cell Biol. 1992 Dec;119(6):1387-94 PMID: 1469039
  47. Neurite growth on different substrates: permissive versus instructive influences and the role of adhesive strength.
    J Neurosci. 1992 Mar;12(3):818-26 PMID: 1545241
  48. A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth.
    Development. 1991 Dec;113(4):1473-85 PMID: 1811954
  49. Peanut agglutinin and chondroitin-6-sulfate are molecular markers for tissues that act as barriers to axon advance in the avian embryo.
    Dev Biol. 1991 Sep;147(1):187-206 PMID: 1908800
  50. Heterotypic binding between neuronal membrane vesicles and glial cells is mediated by a specific cell adhesion molecule.
    J Cell Biol. 1984 May;98(5):1746-56 PMID: 6725397
  51. Neuron-glia cell adhesion molecule interacts with neurons and astroglia via different binding mechanisms.
    J Cell Biol. 1988 Feb;106(2):487-503 PMID: 2448316
  52. Cell Type-specific Effects of the Neural Adhesion Molecules L1 and N-CAM on Diverse Second Messenger Systems.
    Eur J Neurosci. 1992;4(10):896-909 PMID: 12106425
  53. The myelin-associated glycoproteins: membrane disposition, evidence of a novel disulfide linkage between immunoglobulin-like domains, and posttranslational palmitylation.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2651-61 PMID: 1703542
  54. Epidermal growth factor (EGF) induces oligomerization of soluble, extracellular, ligand-binding domain of EGF receptor. A low resolution projection structure of the ligand-binding domain.
    J Biol Chem. 1991 Jul 25;266(21):13828-33 PMID: 1856216
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-05-00
Pages
669-80
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2119998
Subset
IM
Grants
NINDS NIH HHS · NS-09348 · United States
NINDS NIH HHS · NS-13876 · United States
NINDS NIH HHS · NS-21629 · United States
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: [email protected]