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PMID: 1382076 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Neuronal cell adhesion molecule contactin/F11 binds to tenascin via its immunoglobulin-like domains.

The Journal of cell biology ·Vol. 119 ·No. 1 ·1992-10-00 ·Pages 203-13

Zisch AH, D'Alessandri L, Ranscht B, Falchetto R, Winterhalter KH, Vaughan L

Abstract

Adhesive interactions between neurons and extracellular matrix (ECM) play a key role in neuronal pattern formation. The prominent role played by the extracellular matrix protein tenascin/cytotactin in the development of the nervous system, tied to its abundance, led us to speculate that brain may contain yet unidentified tenascin receptors. Here we show that the neuronal cell adhesion molecule contactin/F11, a member of the immunoglobulin(Ig)-superfamily, is a cell surface ligand for tenascin in the nervous system. Through affinity chromatography of membrane glycoproteins from chick brain on tenascin-Sepharose, we isolated a major cell surface ligand of 135 kD which we identified as contactin/F11 by NH2-terminal sequencing. The binding specificity between contactin/F11 and tenascin was demonstrated in solid-phase assays. Binding of immunopurified 125I-labeled contactin/F11 to immobilized tenascin is completely inhibited by the addition of soluble tenascin or contactin/F11, but not by fibronectin. When the fractionated isoforms of tenascin were used as substrates, contactin/F11 bound preferentially to the 190-kD isoform. This isoform differs in having no alternatively spliced fibronectin type III domains. Our results imply that the introduction of these additional domains in some way disrupts the contactin/F11 binding site on tenascin. To localize the binding site on contactin/F11, proteolytic fragments were generated and characterized by NH2-terminal sequencing. The smallest contactin/F11 fragment which binds tenascin is 45 kD and also begins with the contactin/F11 NH2-terminal sequence. This implies that contactin/F11 binds to tenascin through a site within the first three Ig-domains.

MeSH Terms
Amino Acid Sequence Animals Cell Adhesion/physiology Cell Adhesion Molecules, Neuronal/chemistry,metabolism Chick Embryo Chromatography, Affinity Contactins Extracellular Matrix/metabolism Extracellular Matrix Proteins/chemistry,metabolism Immunoglobulins/chemistry Membrane Glycoproteins/chemistry,metabolism Molecular Sequence Data Nerve Tissue Proteins/chemistry,metabolism Peptide Fragments/metabolism Radioligand Assay Tenascin
Chemicals
Cell Adhesion Molecules, Neuronal Contactins Extracellular Matrix Proteins Immunoglobulins Membrane Glycoproteins Nerve Tissue Proteins Peptide Fragments Tenascin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Zisch A H
Laboratorium für Biochemie I, ETH-Zentrum, Zürich, Switzerland.
D'Alessandri L
Ranscht B
Falchetto R
Winterhalter K H
Vaughan L
References (65)
65 references, click to expand
  1. Distribution and function of tenascin during cranial neural crest development in the chick.
    J Neurosci Res. 1988 Oct-Dec;21(2-4):135-47 PMID: 2464073
  2. Fibronectin: purification, immunochemical properties, and biological activities.
    Methods Enzymol. 1982;82 Pt A:803-31 PMID: 7078457
  3. Syndecan from embryonic tooth mesenchyme binds tenascin.
    J Biol Chem. 1991 Apr 25;266(12):7733-9 PMID: 1708391
  4. Differential expression of tenascin splicing variants in the chick gizzard and in cell cultures.
    Cell Differ Dev. 1990 Dec 2;32(3):417-23 PMID: 1711921
  5. Neurite outgrowth on immobilized axonin-1 is mediated by a heterophilic interaction with L1(G4).
    J Cell Biol. 1991 Nov;115(4):1113-26 PMID: 1720120
  6. Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowth in vitro.
    Development. 1990 Oct;110(2):401-15 PMID: 1723942
  7. F3/F11 cell surface molecule expression in the developing mouse cerebellum is polarized at synaptic sites and within granule cells.
    J Neurosci. 1992 Jan;12(1):257-67 PMID: 1729438
  8. Restrictin: a chick neural extracellular matrix protein involved in cell attachment co-purifies with the cell recognition molecule F11.
    Development. 1991 Sep;113(1):151-64 PMID: 1764992
  9. Cell adhesion molecules: implications for a molecular histology.
    Annu Rev Biochem. 1991;60:155-90 PMID: 1883195
  10. Transfected F3/F11 neuronal cell surface protein mediates intercellular adhesion and promotes neurite outgrowth.
    Neuron. 1991 Apr;6(4):595-606 PMID: 2015094
  11. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity.
    Cell. 1990 Apr 6;61(1):157-70 PMID: 2317872
  12. Site-restricted expression of cytotactin during development of the chicken embryo.
    J Cell Biol. 1986 May;102(5):1917-30 PMID: 2422181
  13. Topographic localization of the heparin-binding domain of the neural cell adhesion molecule N-CAM.
    J Cell Biol. 1986 Nov;103(5):1739-44 PMID: 2430978
  14. Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution.
    Proc Natl Acad Sci U S A. 1987 Nov;84(22):7977-81 PMID: 2446315
  15. Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field.
    Dev Biol. 1989 Jan;131(1):243-60 PMID: 2462518
  16. Tenascin mediates cell attachment through an RGD-dependent receptor.
    J Cell Biol. 1989 Mar;108(3):1149-55 PMID: 2466038
  17. The mouse neuronal cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin.
    J Cell Biol. 1989 Aug;109(2):775-88 PMID: 2474555
  18. An alternatively spliced region of the human hexabrachion contains a repeat of potential N-glycosylation sites.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1588-92 PMID: 2466295
  19. A detailed structural model of cytotactin: protein homologies, alternative RNA splicing, and binding regions.
    Proc Natl Acad Sci U S A. 1989 Mar;86(6):1905-9 PMID: 2467292
  20. Tenascin/J1/cytotactin: the potential function of hexabrachion proteins in neural development.
    Dev Neurosci. 1989;11(4-5):266-75 PMID: 2477211
  21. Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse.
    Dev Biol. 1989 Dec;136(2):381-92 PMID: 2479585
  22. J1/tenascin-related molecules are not responsible for the segmented pattern of neural crest cells or motor axons in the chick embryo.
    Development. 1989 Oct;107(2):309-19 PMID: 2483682
  23. Neural cell recognition molecule F11: homology with fibronectin type III and immunoglobulin type C domains.
    Neuron. 1989 Apr;2(4):1351-61 PMID: 2627374
  24. Sequence of contactin, a 130-kD glycoprotein concentrated in areas of interneuronal contact, defines a new member of the immunoglobulin supergene family in the nervous system.
    J Cell Biol. 1988 Oct;107(4):1561-73 PMID: 3049624
  25. Adhesion molecules and the hierarchy of neural development.
    Neuron. 1988 Mar;1(1):3-13 PMID: 3078409
  26. Cell surface receptors for extracellular matrix components.
    Biochim Biophys Acta. 1990 Feb 28;1031(1):91-110 PMID: 1689589
  27. Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis.
    J Cell Biol. 1991 Jan;112(2):355-62 PMID: 1703162
  28. Cell adhesion molecules in vertebrate neural development.
    Physiol Rev. 1988 Jul;68(3):819-57 PMID: 3293093
  29. Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins.
    J Cell Biol. 1987 Feb;104(2):355-62 PMID: 3543026
  30. A major, six-armed glycoprotein from embryonic cartilage.
    EMBO J. 1987 Feb;6(2):349-53 PMID: 3582363
  31. Immunochemical and biochemical characterization of a glioma-associated extracellular matrix glycoprotein.
    J Cell Biochem. 1985;28(3):183-95 PMID: 4066774
  32. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  33. The basis for colored silver-protein complex formation in stained polyacrylamide gels.
    Anal Biochem. 1984 Sep;141(2):311-5 PMID: 6208811
  34. A six-armed oligomer isolated from cell surface fibronectin preparations.
    Nature. 1984 Sep 20-26;311(5983):267-9 PMID: 6482952
  35. Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments.
    Cell. 1989 Oct 20;59(2):325-34 PMID: 2478295
  36. Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors.
    Annu Rev Cell Biol. 1989;5:71-92 PMID: 2480799
  37. L1-mediated axon outgrowth occurs via a homophilic binding mechanism.
    Neuron. 1989 Jun;2(6):1597-603 PMID: 2627381
  38. Mechanisms of vertebrate segmentation.
    Development. 1988 Jul;103(3):413-29 PMID: 3073078
  39. 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
  40. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing.
    Science. 1987 May 15;236(4803):799-806 PMID: 3576199
  41. Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers.
    J Cell Biol. 1987 Feb;104(2):331-42 PMID: 3805122
  42. A neuronal surface glycoprotein associated with the cytoskeleton.
    J Cell Biol. 1984 Nov;99(5):1803-13 PMID: 6208203
  43. Segmentation in the vertebrate nervous system.
    Nature. 1984 Aug 30-Sep 5;310(5980):786-9 PMID: 6472458
  44. Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats.
    J Cell Biol. 1992 Mar;116(6):1475-86 PMID: 1371773
  45. Expression of tenascin in the developing and adult cerebellar cortex.
    J Neurosci. 1992 Mar;12(3):736-49 PMID: 1372043
  46. Localization during development of alternatively spliced forms of cytotactin mRNA by in situ hybridization.
    J Cell Biol. 1990 Aug;111(2):685-98 PMID: 1696267
  47. J1/tenascin is a repulsive substrate for central nervous system neurons.
    Neuron. 1990 Nov;5(5):627-37 PMID: 1699568
  48. 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
  49. 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
  50. Isolation of chick tenascin variants and fragments. A C-terminal heparin-binding fragment produced by cleavage of the extra domain from the largest subunit splicing variant.
    Eur J Biochem. 1991 Jul 15;199(2):379-88 PMID: 1712728
  51. Cytotactin expression in somites after dorsal neural tube and neural crest ablation in chicken embryos.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6398-402 PMID: 1713677
  52. Focal adhesion integrity is downregulated by the alternatively spliced domain of human tenascin.
    J Cell Biol. 1991 Nov;115(4):1127-36 PMID: 1720121
  53. Tenascin Mr 220,000 isoform expression correlates with corneal cell migration.
    Development. 1991 Jun;112(2):605-14 PMID: 1724418
  54. Tenascin variants: differential binding to fibronectin and distinct distribution in cell cultures and tissues.
    Cell Regul. 1991 Nov;2(11):927-38 PMID: 1725601
  55. Chondroitin sulfate as a regulator of neuronal patterning in the retina.
    Science. 1992 Feb 7;255(5045):733-6 PMID: 1738848
  56. Extracellular matrix molecules and their receptors: functions in neural development.
    Annu Rev Neurosci. 1991;14:531-70 PMID: 1851608
  57. The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus.
    Cell. 1990 Apr 20;61(2):243-54 PMID: 1970514
  58. The axonally secreted protein axonin-1 is a potent substratum for neurite growth.
    J Cell Biol. 1991 Feb;112(3):449-55 PMID: 1991792
  59. Binding of the J1 adhesion molecules to extracellular matrix constituents.
    J Neurochem. 1990 Mar;54(3):1004-15 PMID: 2303805
  60. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family.
    Nature. 1985 Jul 11-17;316(6024):146-8 PMID: 2409452
  61. Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):8075-9 PMID: 2415980
  62. Neuronal cell adhesion molecules and cytotactin are colocalized at the node of Ranvier.
    J Cell Biol. 1986 Aug;103(2):379-91 PMID: 2426280
  63. A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin.
    Proc Natl Acad Sci U S A. 1987 Apr;84(8):2523-7 PMID: 2436234
  64. The distribution of tenascin coincides with pathways of neural crest cell migration.
    Development. 1988 Jan;102(1):237-50 PMID: 2458221
  65. Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2341-9 PMID: 2461951
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1992-10-00
Pages
203-13
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2289633
Subset
IM
Grants
NINDS NIH HHS · NS 25194 · United States
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