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PMID: 2474555 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The mouse neuronal cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin.

The Journal of cell biology ·Vol. 109 ·No. 2 ·1989-08-00 ·Pages 775-88

Gennarini G, Cibelli G, Rougon G, Mattei MG, Goridis C

Abstract

Several members of the Ig superfamily are expressed on neural cells where they participate in surface interactions between cell bodies and processes. Their Ig domains are more closely related to each other than to Ig variable and constant domains and have been grouped into the C2 set. Here, we report the cloning and characterization of another member of this group, the mouse neuronal cell surface antigen F3. The F3 cDNA sequence contains an open reading frame that could encode a 1,020-amino acid protein consisting of a signal sequence, six Ig-like domains of the C2 type, a long premembrane region containing two segments that exhibit sequence similarity to fibronectin type III repeats and a moderately hydrophobic COOH-terminal sequence. The protein does not contain a typical transmembrane segment but appears to be attached to the membrane by a phosphatidylinositol anchor. Antibodies against the F3 protein recognize a prominent 135-kD protein in mouse brain. In fetal brain cultures, they stain the neuronal cell surface and, in cultures maintained in chemically defined medium, most prominently neurites and neurite bundles. The mouse f3 gene maps to band F of chromosome 15. The gene transcripts detected in the brain by F3 cDNA probes are developmentally regulated, the highest amounts being expressed between 1 and 2 wk after birth. The F3 nucleotide and deduced amino acid sequence show striking similarity to the recently published sequence of the chicken neuronal cell surface protein contactin. However, there are important differences between the two molecules. In contrast to F3, contactin has a transmembrane and a cytoplasmic domain. Whereas contactin is insoluble in nonionic detergent and is tightly associated with the cytoskeleton, about equal amounts of F3 distribute between buffer-soluble, nonionic detergent-soluble, and detergent-insoluble fractions. Among other neural cell surface proteins, F3 most resembles the neuronal cell adhesion protein L1, with 25% amino acid identity between their extracellular domains. Based on its structural similarity with known cell adhesion proteins of nervous tissue and with L1 in particular, we propose that F3 mediates cell surface interactions during nervous system development.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Blotting, Southern Cell Adhesion Cell Adhesion Molecules, Neuronal Cell Membrane/analysis,metabolism Cells, Cultured Chromosome Mapping Contactin 1 Contactins DNA/analysis,genetics Fibronectins/analysis,genetics Fluorescent Antibody Technique Gene Expression Regulation Genetic Linkage Membrane Proteins/analysis,genetics,isolation & purification Mice Molecular Sequence Data Nerve Tissue Proteins/analysis,genetics,isolation & purification Neurons/analysis,cytology,metabolism Nucleic Acid Hybridization Phosphatidylinositols/metabolism Protein Biosynthesis RNA/genetics,metabolism Receptors, Antigen, B-Cell/analysis,genetics,isolation & purification Sequence Homology, Nucleic Acid Tissue Extracts/analysis,genetics
Chemicals
Cell Adhesion Molecules, Neuronal Cntn1 protein, mouse Contactin 1 Contactins Fibronectins Membrane Proteins Nerve Tissue Proteins Phosphatidylinositols Receptors, Antigen, B-Cell Tissue Extracts RNA DNA
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Gennarini G
Centre d'Immunologie, Marseille, France.
Cibelli G
Rougon G
Mattei M G
Goridis C
References (72)
72 references, click to expand
  1. Monoclonal antibody to neural cell surface protein: identification of a glycoprotein family of restricted cellular localization.
    Neuroscience. 1983 Oct;10(2):511-20 PMID: 6355895
  2. Molecular and biological properties of a neural cell adhesion molecule.
    Cold Spring Harb Symp Quant Biol. 1983;48 Pt 2:501-14 PMID: 6586371
  3. Structure and modulation of neural cell adhesion molecules in early and late embryogenesis.
    Cold Spring Harb Symp Quant Biol. 1983;48 Pt 2:515-26 PMID: 6586372
  4. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum.
    Anal Biochem. 1984 Feb;137(1):266-7 PMID: 6329026
  5. Human fibronectin: cell specific alternative mRNA splicing generates polypeptide chains differing in the number of internal repeats.
    Nucleic Acids Res. 1984 Jul 25;12(14):5853-68 PMID: 6462919
  6. Expression of neural cell adhesion molecule L1 during development, in neurological mutants and in the peripheral nervous system.
    Brain Res. 1984 Jul;317(1):69-82 PMID: 6467033
  7. 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
  8. A neuronal surface glycoprotein associated with the cytoskeleton.
    J Cell Biol. 1984 Nov;99(5):1803-13 PMID: 6208203
  9. The glyceraldehyde 3 phosphate dehydrogenase gene family: structure of a human cDNA and of an X chromosome linked pseudogene; amazing complexity of the gene family in mouse.
    EMBO J. 1984 Nov;3(11):2627-33 PMID: 6096136
  10. T cell antigen receptors and the immunoglobulin supergene family.
    Cell. 1985 Feb;40(2):225-9 PMID: 3917857
  11. A new method for purifying lambda DNA from phage lysates.
    DNA. 1985 Feb;4(1):39-49 PMID: 2982558
  12. Involvement of the nerve growth factor-inducible large external glycoprotein (NILE) in neurite fasciculation in primary cultures of rat brain.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):1276-80 PMID: 3856258
  13. DNA probe localization at 18p113 band by in situ hybridization and identification of a small supernumerary chromosome.
    Hum Genet. 1985;69(3):268-71 PMID: 3980018
  14. 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
  15. Differential inhibition of neurone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies.
    Nature. 1985 Aug 22-28;316(6030):728-30 PMID: 4033770
  16. Repeating modular structure of the fibronectin gene: relationship to protein structure and subunit variation.
    Proc Natl Acad Sci U S A. 1985 Oct;82(19):6571-5 PMID: 3863113
  17. Demonstration of immunochemical identity between the nerve growth factor-inducible large external (NILE) glycoprotein and the cell adhesion molecule L1.
    EMBO J. 1985 Nov;4(11):2765-8 PMID: 2415352
  18. Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1.
    J Neurosci. 1986 Feb;6(2):605-12 PMID: 3512794
  19. Differential distribution of cell adhesion molecules during histogenesis of the chick nervous system.
    J Neurosci. 1986 Mar;6(3):739-58 PMID: 2420947
  20. Adhesion properties of a neuronal epitope recognized by the monoclonal antibody HNK-1.
    Brain Res. 1986 Mar 5;367(1-2):20-5 PMID: 2421830
  21. The molecular genetics of the T-cell antigen receptor and T-cell antigen recognition.
    Annu Rev Immunol. 1986;4:529-91 PMID: 3518750
  22. Differential expression of mouse neural cell-adhesion molecule (N-CAM) mRNA species during brain development and in neural cell lines.
    J Neurosci. 1986 Jul;6(7):1983-90 PMID: 3734870
  23. Characterisation of a soluble trypsin fragment of GP130: a neuronal glycoprotein associated with the cytoskeleton.
    J Cell Biochem. 1986;32(2):97-112 PMID: 3782313
  24. Eukaryotic protein modification and membrane attachment via phosphatidylinositol.
    Cell. 1987 Jan 30;48(2):179-81 PMID: 3542226
  25. Membrane glycoproteins involved in neurite fasciculation.
    J Cell Biol. 1987 Feb;104(2):343-53 PMID: 3805123
  26. Cell adhesion molecules in the regulation of animal form and tissue pattern.
    Annu Rev Cell Biol. 1986;2:81-116 PMID: 3548776
  27. The amino acid sequences of the myelin-associated glycoproteins: homology to the immunoglobulin gene superfamily.
    J Cell Biol. 1987 Apr;104(4):957-65 PMID: 2435742
  28. 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
  29. 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
  30. Visualization of neural cell adhesion molecule by electron microscopy.
    J Cell Biol. 1987 Jun;104(6):1579-86 PMID: 2438287
  31. The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: cell adhesion receptors of the immune system.
    Annu Rev Immunol. 1987;5:223-52 PMID: 3109455
  32. The structure of the CD4 and CD8 genes.
    Annu Rev Immunol. 1987;5:561-84 PMID: 3109457
  33. Isolation and nucleotide sequence of mouse NCAM cDNA that codes for a Mr 79,000 polypeptide without a membrane-spanning region.
    EMBO J. 1987 Apr;6(4):907-14 PMID: 3595563
  34. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  35. The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions.
    Cell Tissue Res. 1987 Oct;250(1):227-36 PMID: 3308110
  36. Biochemistry of the glycosyl-phosphatidylinositol membrane protein anchors.
    Biochem J. 1987 May 15;244(1):1-13 PMID: 2959270
  37. Myelin-associated glycoprotein, a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte-oligodendrocyte interaction.
    J Cell Biol. 1987 Oct;105(4):1893-9 PMID: 2444603
  38. Anchoring mechanisms for LFA-3 cell adhesion glycoprotein at membrane surface.
    Nature. 1987 Oct 29-Nov 4;329(6142):846-8 PMID: 3313053
  39. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs.
    Nucleic Acids Res. 1987 Oct 26;15(20):8125-48 PMID: 3313277
  40. Neurofascin: a novel chick cell-surface glycoprotein involved in neurite-neurite interactions.
    Cell. 1987 Dec 4;51(5):841-9 PMID: 3677174
  41. Biosynthesis, membrane association, and release of N-CAM-120, a phosphatidylinositol-linked form of the neural cell adhesion molecule.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2489-500 PMID: 3693391
  42. The L2/HNK-1 carbohydrate of neural cell adhesion molecules is involved in cell interactions.
    J Cell Biol. 1988 Jan;106(1):213-23 PMID: 2448311
  43. 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
  44. CAMs and Igs: cell adhesion and the evolutionary origins of immunity.
    Immunol Rev. 1987 Dec;100:11-45 PMID: 3326819
  45. Neural protein 1B236/myelin-associated glycoprotein (MAG) defines a subgroup of the immunoglobulin superfamily.
    Immunol Rev. 1987 Dec;100:129-51 PMID: 2450062
  46. Site-directed mutagenesis of the cell-binding domain of human fibronectin: separable, synergistic sites mediate adhesive function.
    Cell. 1988 May 20;53(4):649-57 PMID: 3286012
  47. Structure and function of human and murine receptors for IgG.
    Annu Rev Immunol. 1988;6:251-81 PMID: 2968084
  48. The immunoglobulin superfamily--domains for cell surface recognition.
    Annu Rev Immunol. 1988;6:381-405 PMID: 3289571
  49. Cell adhesion molecules in vertebrate neural development.
    Physiol Rev. 1988 Jul;68(3):819-57 PMID: 3293093
  50. Differential splicing and alternative polyadenylation generates distinct NCAM transcripts and proteins in the mouse.
    EMBO J. 1988 Mar;7(3):625-32 PMID: 3396534
  51. 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
  52. Cell membrane, but not circulating, carcinoembryonic antigen is linked to a phosphatidylinositol-containing hydrophobic domain.
    Biochem Biophys Res Commun. 1988 Sep 15;155(2):794-800 PMID: 3048262
  53. 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
  54. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures.
    Annu Rev Biochem. 1988;57:285-320 PMID: 3052274
  55. Characterization of amalgam: a member of the immunoglobulin superfamily from Drosophila.
    Cell. 1988 Nov 18;55(4):589-600 PMID: 3141062
  56. Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily.
    Science. 1988 Nov 4;242(4879):700-8 PMID: 3187519
  57. Alternative splicing generates a secreted form of N-CAM in muscle and brain.
    Cell. 1988 Dec 23;55(6):955-64 PMID: 3203385
  58. Identification and cDNA cloning of a new member of the L2/HNK-1 family of neural surface glycoproteins.
    J Neurosci Res. 1989 Jan;22(1):1-12 PMID: 2926836
  59. Isolation and analysis of the gene encoding peripheral myelin protein zero.
    Neuron. 1988 Mar;1(1):73-83 PMID: 2483091
  60. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons.
    Neuron. 1988 Apr;1(2):105-16 PMID: 3272160
  61. Neural cell recognition molecule F11: homology with fibronectin type III and immunoglobulin type C domains.
    Neuron. 1989 Apr;2(4):1351-61 PMID: 2627374
  62. Neural surface antigens during nervous system development.
    Cold Spring Harb Symp Quant Biol. 1983;48 Pt 2:527-37 PMID: 6586373
  63. The covalent structure of a human gamma G-immunoglobulin. XI. Functional implications.
    Biochemistry. 1970 Aug 4;9(16):3197-205 PMID: 5489773
  64. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  65. Three-dimensional structure of immunoglobulins.
    Annu Rev Biochem. 1979;48:961-97 PMID: 89832
  66. Purification and properties of phosphatidylinositol-specific phospholipase C of Bacillus thuringiensis.
    Biochim Biophys Acta. 1980 Jul 14;619(1):48-57 PMID: 7417468
  67. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201-5 PMID: 6159641
  68. Pattern recognition in nucleic acid sequences. I. A general method for finding local homologies and symmetries.
    Nucleic Acids Res. 1982 Jan 11;10(1):247-63 PMID: 6801626
  69. Partial primary structure of bovine plasma fibronectin: three types of internal homology.
    Proc Natl Acad Sci U S A. 1983 Jan;80(1):137-41 PMID: 6218503
  70. Patterns of amino acids near signal-sequence cleavage sites.
    Eur J Biochem. 1983 Jun 1;133(1):17-21 PMID: 6852022
  71. Establishing homologies in protein sequences.
    Methods Enzymol. 1983;91:524-45 PMID: 6855599
  72. Cytoskeleton-associated glycoproteins from chicken sympathetic neurons and chicken embryo brain.
    Eur J Biochem. 1983 Sep 15;135(2):291-7 PMID: 6684040
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.109.2.775
Published
1989-08-00
Pages
775-88
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2115732
Subset
IM
Databases
GENBANK
X14943
External Links
PubMed source DOI: 10.1083/jcb.109.2.775 PMC Full Text View journal details
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