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. 1986 Mar 1;102(3):844–852. doi: 10.1083/jcb.102.3.844

Molecular specialization of astrocyte processes at nodes of Ranvier in rat optic nerve

PMCID: PMC2114143  PMID: 2419343

Abstract

The HNK-1 and L2 monoclonal antibodies are thought to recognize identical or closely associated carbohydrate epitopes on a family of neural plasma membrane glycoproteins, including myelin-associated glycoprotein, the neural cell adhesion molecule, and the L1 and J1 glycoproteins, all of which have been postulated to play a part in mediating cell-cell interactions in the nervous system. We have used these two antibodies in immunofluorescence and immunogold-electron microscopic studies of semithin and ultrathin frozen sections of adult rat optic nerve, respectively, and we show that they bind mainly to astrocyte processes around nodes of Ranvier. Most other elements of the nerve, including astrocyte cell bodies and large astrocytic processes, are not labeled by the antibodies. To our knowledge, this is the first demonstration that perinodal astrocyte processes are biochemically specialized. We provide evidence that one of the HNK-1+/L2+ molecules concentrated around perinodal astrocyte processes is the J1 glycoprotein; our findings, taken together with previously reported observations, suggest that the other known HNK-1+/L2+ molecules are not concentrated on these processes. Since anti-J1 antibodies previously have been shown to inhibit neuron to astrocyte adhesion in vitro, we hypothesize that J1 may play an important part in the axon-glial interactions that presumably are involved in the assembly and/or maintenance of nodes of Ranvier.

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Selected References

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  1. Abo T., Balch C. M. A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol. 1981 Sep;127(3):1024–1029. [PubMed] [Google Scholar]
  2. Anderton B. H., Thorpe R., Cohen J., Selvendran S., Woodhams P. Specific neuronal localization by immunofluorescence of 10 nm filament polypeptides. J Neurocytol. 1980 Dec;9(6):835–844. doi: 10.1007/BF01205022. [DOI] [PubMed] [Google Scholar]
  3. Black J. A., Waxman S. G., Hildebrand C. Membrane specialization and axo-glial association in the rat retinal nerve fibre layer: freeze-fracture observations. J Neurocytol. 1984 Jun;13(3):417–430. doi: 10.1007/BF01148332. [DOI] [PubMed] [Google Scholar]
  4. Edelman G. M. Cell adhesion molecules. Science. 1983 Feb 4;219(4584):450–457. doi: 10.1126/science.6823544. [DOI] [PubMed] [Google Scholar]
  5. Gotow T. Cytochemical characteristics of astrocytic plasma membranes specialized with numerous orthogonal arrays. J Neurocytol. 1984 Jun;13(3):431–448. doi: 10.1007/BF01148333. [DOI] [PubMed] [Google Scholar]
  6. Habu S., Raff M. C. Accessory cell dependence of lectin-induced proliferation of mouse T lymphocytes. Eur J Immunol. 1977 Jul;7(7):451–457. doi: 10.1002/eji.1830070710. [DOI] [PubMed] [Google Scholar]
  7. Haimovich B., Bonilla E., Casadei J., Barchi R. Immunocytochemical localization of the mammalian voltage-dependent sodium channel using polyclonal antibodies against the purified protein. J Neurosci. 1984 Sep;4(9):2259–2268. doi: 10.1523/JNEUROSCI.04-09-02259.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hildebrand C., Waxman S. G. Postnatal differentiation of rat optic nerve fibers: electron microscopic observations on the development of nodes of Ranvier and axoglial relations. J Comp Neurol. 1984 Mar 20;224(1):25–37. doi: 10.1002/cne.902240103. [DOI] [PubMed] [Google Scholar]
  9. Huxley A. F., Stämpfli R. Evidence for saltatory conduction in peripheral myelinated nerve fibres. J Physiol. 1949 May 15;108(3):315–339. [PMC free article] [PubMed] [Google Scholar]
  10. Johnson G. D., Davidson R. S., McNamee K. C., Russell G., Goodwin D., Holborow E. J. Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy. J Immunol Methods. 1982 Dec 17;55(2):231–242. doi: 10.1016/0022-1759(82)90035-7. [DOI] [PubMed] [Google Scholar]
  11. Keilhauer G., Faissner A., Schachner M. Differential inhibition of neurone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature. 1985 Aug 22;316(6030):728–730. doi: 10.1038/316728a0. [DOI] [PubMed] [Google Scholar]
  12. Keller G. A., Tokuyasu K. T., Dutton A. H., Singer S. J. An improved procedure for immunoelectron microscopy: ultrathin plastic embedding of immunolabeled ultrathin frozen sections. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5744–5747. doi: 10.1073/pnas.81.18.5744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Kruse J., Mailhammer R., Wernecke H., Faissner A., Sommer I., Goridis C., Schachner M. 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;311(5982):153–155. doi: 10.1038/311153a0. [DOI] [PubMed] [Google Scholar]
  15. Landis D. M., Reese T. S. Regional organization of astrocytic membranes in cerebellar cortex. Neuroscience. 1982 Apr;7(4):937–950. doi: 10.1016/0306-4522(82)90053-7. [DOI] [PubMed] [Google Scholar]
  16. Lawson D. Epinemin: a new protein associated with vimentin filaments in non-neural cells. J Cell Biol. 1983 Dec;97(6):1891–1905. doi: 10.1083/jcb.97.6.1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lindner J., Rathjen F. G., Schachner M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. 1983 Sep 29-Oct 5Nature. 305(5933):427–430. doi: 10.1038/305427a0. [DOI] [PubMed] [Google Scholar]
  18. McGarry R. C., Helfand S. L., Quarles R. H., Roder J. C. Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature. 1983 Nov 24;306(5941):376–378. doi: 10.1038/306376a0. [DOI] [PubMed] [Google Scholar]
  19. Miller R. H., Raff M. C. Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct. J Neurosci. 1984 Feb;4(2):585–592. doi: 10.1523/JNEUROSCI.04-02-00585.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miller R. H., Williams B. P., Cohen J., Raff M. C. A4: an antigenic marker of neural tube-derived cells. J Neurocytol. 1984 Jun;13(3):329–338. doi: 10.1007/BF01148326. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Pruss R. M. Thy-1 antigen on astrocytes in long-term cultures of rat central nervous system. Nature. 1979 Aug 23;280(5724):688–690. doi: 10.1038/280688a0. [DOI] [PubMed] [Google Scholar]
  23. Quarles R. H. Myelin-associated glycoprotein in development and disease. Dev Neurosci. 1983;6(6):285–303. doi: 10.1159/000112356. [DOI] [PubMed] [Google Scholar]
  24. Raine C. S. On the association between perinodal astrocytic processes and the node of Ranvier in the C.N.S. J Neurocytol. 1984 Feb;13(1):21–27. doi: 10.1007/BF01148316. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Ritchie J. M., Rogart R. B. Density of sodium channels in mammalian myelinated nerve fibers and nature of the axonal membrane under the myelin sheath. Proc Natl Acad Sci U S A. 1977 Jan;74(1):211–215. doi: 10.1073/pnas.74.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rosenbluth J. Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain. J Neurocytol. 1976 Dec;5(6):731–745. doi: 10.1007/BF01181584. [DOI] [PubMed] [Google Scholar]
  28. Rutishauser U. Developmental biology of a neural cell adhesion molecule. Nature. 1984 Aug 16;310(5978):549–554. doi: 10.1038/310549a0. [DOI] [PubMed] [Google Scholar]
  29. Schuller-Petrovic S., Gebhart W., Lassmann H., Rumpold H., Kraft D. A shared antigenic determinant between natural killer cells and nervous tissue. Nature. 1983 Nov 10;306(5939):179–181. doi: 10.1038/306179a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Tokuyasu K. T. A study of positive staining of ultrathin frozen sections. J Ultrastruct Res. 1978 Jun;63(3):287–307. doi: 10.1016/s0022-5320(78)80053-7. [DOI] [PubMed] [Google Scholar]
  32. Tokuyasu K. T. A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol. 1973 May;57(2):551–565. doi: 10.1083/jcb.57.2.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vulliamy T., Rattray S., Mirsky R. Cell-surface antigen distinguishes sensory and autonomic peripheral neurones from central neurones. Nature. 1981 Jun 4;291(5814):418–420. doi: 10.1038/291418a0. [DOI] [PubMed] [Google Scholar]
  34. Waxman S. G., Black J. A. Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions. Brain Res. 1984 Aug 6;308(1):77–87. doi: 10.1016/0006-8993(84)90919-3. [DOI] [PubMed] [Google Scholar]
  35. Waxman S. G., Foster R. E. Ionic channel distribution and heterogeneity of the axon membrane in myelinated fibers. Brain Res. 1980 Oct;203(2):205–234. doi: 10.1016/0165-0173(80)90008-9. [DOI] [PubMed] [Google Scholar]
  36. Wernecke H., Lindner J., Schachner M. Cell type specificity and developmental expression of the L2/HNK-1 epitopes in mouse cerebellum. J Neuroimmunol. 1985 Aug;9(3-4):115–130. doi: 10.1016/s0165-5728(85)80012-6. [DOI] [PubMed] [Google Scholar]
  37. Wood J. G., Jean D. H., Whitaker J. N., McLaughlin B. J., Albers R. W. Immunocytochemical localization of the sodium, potassium activated ATPase in knifefish brain. J Neurocytol. 1977 Oct;6(5):571–581. doi: 10.1007/BF01205220. [DOI] [PubMed] [Google Scholar]
  38. Wood J. N., Anderton B. H. Monoclonal antibodies to mammalian neurofilaments. Biosci Rep. 1981 Mar;1(3):263–268. doi: 10.1007/BF01114913. [DOI] [PubMed] [Google Scholar]

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