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. 1993 Mar 1;120(5):1237–1249. doi: 10.1083/jcb.120.5.1237

Molecular characterization and in situ mRNA localization of the neural recognition molecule J1-160/180: a modular structure similar to tenascin

PMCID: PMC2119727  PMID: 7679676

Abstract

The oligodendrocyte-derived extracellular matrix glycoprotein J1- 160/180 is a recognition molecule expressed exclusively in the central nervous system. J1-160/180 has been shown to be adhesive for astrocytes and repellent towards neurons and growth cones. We report here the complete nucleotide sequence of J1-160/180 in the rat. The predicted amino acid sequence showed a structural architecture very similar to tenascin: a cysteine-rich amino terminal region is followed by 4.5 epidermal growth factor-like repeats, 9 fibronectin type III homologous repeats and a domain homologous to fibrinogen. Sequence comparison analysis revealed highest homology of rat J1-160/180 to mouse tenascin and chicken restrictin with a similarity of 66% and 85%, respectively. The J1-160/180-coding mRNA is derived from a single copy gene. Using the polymerase chain reaction we could show that two J1-160/180 isoforms are generated by alternative splicing of the sixth fibronectin type III homologous repeat. Localization of J1-160/180 mRNA by in situ hybridization in the cerebellum, hippocampus and olfactory bulb confirmed the expression of J1-160/180 by oligodendrocytes with a peak of transcription at 7-14 d after birth, indicating a functional role during myelination. In addition, J1-160/180-specific RNA was found in a small subset of neurons in all three structures of the CNS analyzed. These neurons continue to express J1-160/180 in the adult.

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Selected References

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  1. Amaral D. G., Witter M. P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience. 1989;31(3):571–591. doi: 10.1016/0306-4522(89)90424-7. [DOI] [PubMed] [Google Scholar]
  2. Bartsch S., Bartsch U., Dörries U., Faissner A., Weller A., Ekblom P., Schachner M. Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci. 1992 Mar;12(3):736–749. doi: 10.1523/JNEUROSCI.12-03-00736.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  4. Cox E. C., Müller B., Bonhoeffer F. Axonal guidance in the chick visual system: posterior tectal membranes induce collapse of growth cones from the temporal retina. Neuron. 1990 Jan;4(1):31–37. doi: 10.1016/0896-6273(90)90441-h. [DOI] [PubMed] [Google Scholar]
  5. Davies J. A., Cook G. M., Stern C. D., Keynes R. J. Isolation from chick somites of a glycoprotein fraction that causes collapse of dorsal root ganglion growth cones. Neuron. 1990 Jan;4(1):11–20. doi: 10.1016/0896-6273(90)90439-m. [DOI] [PubMed] [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edelman G. M. Cell adhesion molecules in the regulation of animal form and tissue pattern. Annu Rev Cell Biol. 1986;2:81–116. doi: 10.1146/annurev.cb.02.110186.000501. [DOI] [PubMed] [Google Scholar]
  8. Erickson H. P., Bourdon M. A. Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annu Rev Cell Biol. 1989;5:71–92. doi: 10.1146/annurev.cb.05.110189.000443. [DOI] [PubMed] [Google Scholar]
  9. Erickson H. P., Inglesias J. L. A six-armed oligomer isolated from cell surface fibronectin preparations. Nature. 1984 Sep 20;311(5983):267–269. doi: 10.1038/311267a0. [DOI] [PubMed] [Google Scholar]
  10. Faissner A., Kruse J., Chiquet-Ehrismann R., Mackie E. The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation. 1988;37(2):104–114. doi: 10.1111/j.1432-0436.1988.tb00802.x. [DOI] [PubMed] [Google Scholar]
  11. Faissner A., Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron. 1990 Nov;5(5):627–637. doi: 10.1016/0896-6273(90)90217-4. [DOI] [PubMed] [Google Scholar]
  12. Fawcett J. W., Fersht N., Housden L., Schachner M., Pesheva P. Axonal growth on astrocytes is not inhibited by oligodendrocytes. J Cell Sci. 1992 Oct;103(Pt 2):571–579. doi: 10.1242/jcs.103.2.571. [DOI] [PubMed] [Google Scholar]
  13. Fuss B., Pott U., Fischer P., Schwab M. E., Schachner M. Identification of a cDNA clone specific for the oligodendrocyte-derived repulsive extracellular matrix molecule J1-160/180. J Neurosci Res. 1991 Jul;29(3):299–307. doi: 10.1002/jnr.490290305. [DOI] [PubMed] [Google Scholar]
  14. Gatchalian C. L., Schachner M., Sanes J. R. Fibroblasts that proliferate near denervated synaptic sites in skeletal muscle synthesize the adhesive molecules tenascin(J1), N-CAM, fibronectin, and a heparan sulfate proteoglycan. J Cell Biol. 1989 May;108(5):1873–1890. doi: 10.1083/jcb.108.5.1873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gribskov M., Burgess R. R. Sigma factors from E. coli, B. subtilis, phage SP01, and phage T4 are homologous proteins. Nucleic Acids Res. 1986 Aug 26;14(16):6745–6763. doi: 10.1093/nar/14.16.6745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gulcher J. R., Alexakos M. J., Le Beau M. M., Lemons R. S., Stefansson K. Chromosomal localization of the human hexabrachion (tenascin) gene and evidence for recent reduplication within the gene. Genomics. 1990 Apr;6(4):616–622. doi: 10.1016/0888-7543(90)90495-g. [DOI] [PubMed] [Google Scholar]
  17. Gulcher J. R., Nies D. E., Alexakos M. J., Ravikant N. A., Sturgill M. E., Marton L. S., Stefansson K. Structure of the human hexabrachion (tenascin) gene. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9438–9442. doi: 10.1073/pnas.88.21.9438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jessell T. M. Adhesion molecules and the hierarchy of neural development. Neuron. 1988 Mar;1(1):3–13. doi: 10.1016/0896-6273(88)90204-8. [DOI] [PubMed] [Google Scholar]
  19. Jones F. S., Hoffman S., Cunningham B. A., Edelman G. M. 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):1905–1909. doi: 10.1073/pnas.86.6.1905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Keynes R. J., Cook G. M. Repellent cues in axon guidance. Curr Opin Neurobiol. 1992 Feb;2(1):55–59. doi: 10.1016/0959-4388(92)90162-e. [DOI] [PubMed] [Google Scholar]
  21. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kruse J., Keilhauer G., Faissner A., Timpl R., Schachner M. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature. 1985 Jul 11;316(6024):146–148. doi: 10.1038/316146a0. [DOI] [PubMed] [Google Scholar]
  23. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  24. Lai C., Brow M. A., Nave K. A., Noronha A. B., Quarles R. H., Bloom F. E., Milner R. J., Sutcliffe J. G. Two forms of 1B236/myelin-associated glycoprotein, a cell adhesion molecule for postnatal neural development, are produced by alternative splicing. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4337–4341. doi: 10.1073/pnas.84.12.4337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lawler J., Weinstein R., Hynes R. O. Cell attachment to thrombospondin: the role of ARG-GLY-ASP, calcium, and integrin receptors. J Cell Biol. 1988 Dec;107(6 Pt 1):2351–2361. doi: 10.1083/jcb.107.6.2351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moos M., Tacke R., Scherer H., Teplow D., Früh K., Schachner M. Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature. 1988 Aug 25;334(6184):701–703. doi: 10.1038/334701a0. [DOI] [PubMed] [Google Scholar]
  27. Noble M., Albrechtsen M., Møller C., Lyles J., Bock E., Goridis C., Watanabe M., Rutishauser U. Glial cells express N-CAM/D2-CAM-like polypeptides in vitro. Nature. 1985 Aug 22;316(6030):725–728. doi: 10.1038/316725a0. [DOI] [PubMed] [Google Scholar]
  28. Noble M. Points of controversy in the O-2A lineage: clocks and type-2 astrocytes. Glia. 1991;4(2):157–164. doi: 10.1002/glia.440040207. [DOI] [PubMed] [Google Scholar]
  29. Nörenberg U., Wille H., Wolff J. M., Frank R., Rathjen F. G. The chicken neural extracellular matrix molecule restrictin: similarity with EGF-, fibronectin type III-, and fibrinogen-like motifs. Neuron. 1992 May;8(5):849–863. doi: 10.1016/0896-6273(92)90199-n. [DOI] [PubMed] [Google Scholar]
  30. Obar R. A., Collins C. A., Hammarback J. A., Shpetner H. S., Vallee R. B. Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature. 1990 Sep 20;347(6290):256–261. doi: 10.1038/347256a0. [DOI] [PubMed] [Google Scholar]
  31. Persohn E., Schachner M. Immunoelectron microscopic localization of the neural cell adhesion molecules L1 and N-CAM during postnatal development of the mouse cerebellum. J Cell Biol. 1987 Jul;105(1):569–576. doi: 10.1083/jcb.105.1.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pesheva P., Spiess E., Schachner M. J1-160 and J1-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion. J Cell Biol. 1989 Oct;109(4 Pt 1):1765–1778. doi: 10.1083/jcb.109.4.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Prieto A. L., Jones F. S., Cunningham B. A., Crossin K. L., Edelman G. M. Localization during development of alternatively spliced forms of cytotactin mRNA by in situ hybridization. J Cell Biol. 1990 Aug;111(2):685–698. doi: 10.1083/jcb.111.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rathjen F. G., Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 1984 Jan;3(1):1–10. doi: 10.1002/j.1460-2075.1984.tb01753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rathjen F. G., Wolff J. M., Chiquet-Ehrismann R. Restrictin: a chick neural extracellular matrix protein involved in cell attachment co-purifies with the cell recognition molecule F11. Development. 1991 Sep;113(1):151–164. doi: 10.1242/dev.113.1.151. [DOI] [PubMed] [Google Scholar]
  36. Reynolds R., Wilkin G. P. Development of macroglial cells in rat cerebellum. II. An in situ immunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development. 1988 Feb;102(2):409–425. doi: 10.1242/dev.102.2.409. [DOI] [PubMed] [Google Scholar]
  37. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  38. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schlosshauer B. Purification of neuronal cell surface proteins and generation of epitope-specific monoclonal antibodies against cell adhesion molecules. J Neurochem. 1989 Jan;52(1):82–92. doi: 10.1111/j.1471-4159.1989.tb10901.x. [DOI] [PubMed] [Google Scholar]
  40. Schwab M. E. Myelin-associated inhibitors of neurite growth and regeneration in the CNS. Trends Neurosci. 1990 Nov;13(11):452–456. doi: 10.1016/0166-2236(90)90098-u. [DOI] [PubMed] [Google Scholar]
  41. Seilheimer B., Schachner M. Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture. J Cell Biol. 1988 Jul;107(1):341–351. doi: 10.1083/jcb.107.1.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Siri A., Carnemolla B., Saginati M., Leprini A., Casari G., Baralle F., Zardi L. Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acids Res. 1991 Feb 11;19(3):525–531. doi: 10.1093/nar/19.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Spring J., Beck K., Chiquet-Ehrismann R. Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell. 1989 Oct 20;59(2):325–334. doi: 10.1016/0092-8674(89)90294-8. [DOI] [PubMed] [Google Scholar]
  44. Sternberger N. H., Quarles R. H., Itoyama Y., Webster H. D. Myelin-associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rat. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1510–1514. doi: 10.1073/pnas.76.3.1510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Weller A., Beck S., Ekblom P. Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J Cell Biol. 1991 Jan;112(2):355–362. doi: 10.1083/jcb.112.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wenger R. H., Ayane M., Bose R., Köhler G., Nielsen P. J. The genes for a mouse hematopoietic differentiation marker called the heat-stable antigen. Eur J Immunol. 1991 Apr;21(4):1039–1046. doi: 10.1002/eji.1830210427. [DOI] [PubMed] [Google Scholar]
  47. Williams B. P., Read J., Price J. The generation of neurons and oligodendrocytes from a common precursor cell. Neuron. 1991 Oct;7(4):685–693. doi: 10.1016/0896-6273(91)90381-9. [DOI] [PubMed] [Google Scholar]
  48. Wing D. R., Rademacher T. W., Schmitz B., Schachner M., Dwek R. A. Comparative glycosylation in neural adhesion molecules. Biochem Soc Trans. 1992 May;20(2):386–390. doi: 10.1042/bst0200386. [DOI] [PubMed] [Google Scholar]
  49. von Heijne G. Transcending the impenetrable: how proteins come to terms with membranes. Biochim Biophys Acta. 1988 Jun 9;947(2):307–333. doi: 10.1016/0304-4157(88)90013-5. [DOI] [PubMed] [Google Scholar]

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