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. 1992 May 1;117(3):617–627. doi: 10.1083/jcb.117.3.617

Expression of unique sets of GPI-linked proteins by different primary neurons in vitro

PMCID: PMC2289446  PMID: 1349305

Abstract

We have surveyed the proteins expressed at the surface of different primary neurons as a first step in elucidating how axons regulate their ensheathment by glial cells. We characterized the surface proteins of dorsal root ganglion neurons, superior cervical ganglion neurons, and cerebellar granule cells which are myelinated, ensheathed but unmyelinated, and unensheathed, respectively. We found that the most abundant proteins are common to all three types of neurons. Reproducible differences in the composition of the integral membrane proteins (enriched by partitioning into a Triton X-114 detergent phase) were detected. These differences were most striking when the expression of glycosylphosphatidyl-inositol (GPI)-anchored membrane proteins by these different neurons was compared. Variations in the relative abundance and degree of glycosylation of several well known GPI- anchored proteins, including Thy-1, F3/F11, and the 120-kD form of the neural cell adhesion molecule (N-CAM), and an abundant 60-kD GPI-linked protein were observed. In addition, we have identified several potentially novel GPI-anchored glycoproteins on each class of neurons. These include a protein that is present only on superior cervical ganglion neurons and is 90 kD; an abundant protein of 69 kD that is essentially restricted in its expression to dorsal root ganglion neurons; and proteins of 38 and 31 kD that are expressed only on granule cell neurons. Finally, the relative abundance of the three major isoforms of N-CAM was found to vary significantly between these different primary neurons. These results are the first demonstration that nerve fibers with diverse ensheathment fates differ significantly in the composition of their surface proteins and suggest an important role for GPI-anchored proteins in generating diversity of the neuronal cell surface.

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Selected References

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  1. Aguayo A. J., Epps J., Charron L., Bray G. M. Multipotentiality of Schwann cells in cross-anastomosed and grafted myelinated and unmyelinated nerves: quantitative microscopy and radioautography. Brain Res. 1976 Mar 5;104(1):1–20. doi: 10.1016/0006-8993(76)90643-0. [DOI] [PubMed] [Google Scholar]
  2. Bendheim P. E., Brown H. R., Rudelli R. D., Scala L. J., Goller N. L., Wen G. Y., Kascsak R. J., Cashman N. R., Bolton D. C. Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology. 1992 Jan;42(1):149–156. doi: 10.1212/wnl.42.1.149. [DOI] [PubMed] [Google Scholar]
  3. Bhat S., Silberberg D. H. Developmental expression of neural cell adhesion molecules of oligodendrocytes in vivo and in culture. J Neurochem. 1988 Jun;50(6):1830–1838. doi: 10.1111/j.1471-4159.1988.tb02485.x. [DOI] [PubMed] [Google Scholar]
  4. Bixby J. L., Lilien J., Reichardt L. F. Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J Cell Biol. 1988 Jul;107(1):353–361. doi: 10.1083/jcb.107.1.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bolin L. M., Rouse R. V. Localization of Thy-1 expression during postnatal development of the mouse cerebellar cortex. J Neurocytol. 1986 Feb;15(1):29–36. doi: 10.1007/BF02057902. [DOI] [PubMed] [Google Scholar]
  6. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem. 1981 Feb 25;256(4):1604–1607. [PubMed] [Google Scholar]
  7. Brümmendorf T., Wolff J. M., Frank R., Rathjen F. G. Neural cell recognition molecule F11: homology with fibronectin type III and immunoglobulin type C domains. Neuron. 1989 Apr;2(4):1351–1361. doi: 10.1016/0896-6273(89)90073-1. [DOI] [PubMed] [Google Scholar]
  8. Chan P. Y., Lawrence M. B., Dustin M. L., Ferguson L. M., Golan D. E., Springer T. A. Influence of receptor lateral mobility on adhesion strengthening between membranes containing LFA-3 and CD2. J Cell Biol. 1991 Oct;115(1):245–255. doi: 10.1083/jcb.115.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chang S., Rathjen F. G., Raper J. A. Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J Cell Biol. 1987 Feb;104(2):355–362. doi: 10.1083/jcb.104.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cho T. M., Hasegawa J., Ge B. L., Loh H. H. Purification to apparent homogeneity of a mu-type opioid receptor from rat brain. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4138–4142. doi: 10.1073/pnas.83.12.4138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chuong C. M., Edelman G. M. Alterations in neural cell adhesion molecules during development of different regions of the nervous system. J Neurosci. 1984 Sep;4(9):2354–2368. doi: 10.1523/JNEUROSCI.04-09-02354.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cunningham B. A., Hemperly J. J., Murray B. A., Prediger E. A., Brackenbury R., Edelman G. M. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987 May 15;236(4803):799–806. doi: 10.1126/science.3576199. [DOI] [PubMed] [Google Scholar]
  13. Davis S., Aldrich T. H., Valenzuela D. M., Wong V. V., Furth M. E., Squinto S. P., Yancopoulos G. D. The receptor for ciliary neurotrophic factor. Science. 1991 Jul 5;253(5015):59–63. doi: 10.1126/science.1648265. [DOI] [PubMed] [Google Scholar]
  14. Dodd J., Morton S. B., Karagogeos D., Yamamoto M., Jessell T. M. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron. 1988 Apr;1(2):105–116. doi: 10.1016/0896-6273(88)90194-8. [DOI] [PubMed] [Google Scholar]
  15. Dotti C. G., Parton R. G., Simons K. Polarized sorting of glypiated proteins in hippocampal neurons. Nature. 1991 Jan 10;349(6305):158–161. doi: 10.1038/349158a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Eldridge C. F., Bunge M. B., Bunge R. P. Differentiation of axon-related Schwann cells in vitro: II. Control of myelin formation by basal lamina. J Neurosci. 1989 Feb;9(2):625–638. doi: 10.1523/JNEUROSCI.09-02-00625.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Estridge M., Bunge R. Compositional analysis of growing axons from rat sympathetic neurons. J Cell Biol. 1978 Oct;79(1):138–155. doi: 10.1083/jcb.79.1.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Faivre-Sarrailh C., Gennarini G., Goridis C., Rougon G. 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):257–267. doi: 10.1523/JNEUROSCI.12-01-00257.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ferguson M. A., Williams A. F. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annu Rev Biochem. 1988;57:285–320. doi: 10.1146/annurev.bi.57.070188.001441. [DOI] [PubMed] [Google Scholar]
  21. Friede R. L. Control of myelin formation by axon caliber (with a model of the control mechanism). J Comp Neurol. 1972 Feb;144(2):233–252. doi: 10.1002/cne.901440207. [DOI] [PubMed] [Google Scholar]
  22. Furley A. J., Morton S. B., Manalo D., Karagogeos D., Dodd J., Jessell T. M. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell. 1990 Apr 6;61(1):157–170. doi: 10.1016/0092-8674(90)90223-2. [DOI] [PubMed] [Google Scholar]
  23. Gennarini G., Cibelli G., Rougon G., Mattei M. G., Goridis C. 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):775–788. doi: 10.1083/jcb.109.2.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gennarini G., Durbec P., Boned A., Rougon G., Goridis C. Transfected F3/F11 neuronal cell surface protein mediates intercellular adhesion and promotes neurite outgrowth. Neuron. 1991 Apr;6(4):595–606. doi: 10.1016/0896-6273(91)90062-5. [DOI] [PubMed] [Google Scholar]
  25. He H. T., Finne J., Goridis C. 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):2489–2500. doi: 10.1083/jcb.105.6.2489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hemperly J. J., Edelman G. M., Cunningham B. A. cDNA clones of the neural cell adhesion molecule (N-CAM) lacking a membrane-spanning region consistent with evidence for membrane attachment via a phosphatidylinositol intermediate. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9822–9826. doi: 10.1073/pnas.83.24.9822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Herndon M. E., Lander A. D. A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron. 1990 Jun;4(6):949–961. doi: 10.1016/0896-6273(90)90148-9. [DOI] [PubMed] [Google Scholar]
  28. Hortsch M., Goodman C. S. Drosophila fasciclin I, a neural cell adhesion molecule, has a phosphatidylinositol lipid membrane anchor that is developmentally regulated. J Biol Chem. 1990 Sep 5;265(25):15104–15109. [PubMed] [Google Scholar]
  29. Hubbard A. L., Cohn Z. A. The enzymatic iodination of the red cell membrane. J Cell Biol. 1972 Nov;55(2):390–405. doi: 10.1083/jcb.55.2.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ishihara A., Hou Y., Jacobson K. The Thy-1 antigen exhibits rapid lateral diffusion in the plasma membrane of rodent lymphoid cells and fibroblasts. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1290–1293. doi: 10.1073/pnas.84.5.1290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Jessell T. M., Hynes M. A., Dodd J. Carbohydrates and carbohydrate-binding proteins in the nervous system. Annu Rev Neurosci. 1990;13:227–255. doi: 10.1146/annurev.ne.13.030190.001303. [DOI] [PubMed] [Google Scholar]
  32. Johnson M. I., Iacovitti L., Higgins D., Bunge R. P., Burton H. Growth and development of sympathetic neurons in tissue culture. Ciba Found Symp. 1981;83:108–122. doi: 10.1002/9780470720653.ch6. [DOI] [PubMed] [Google Scholar]
  33. Karagogeos D., Morton S. B., Casano F., Dodd J., Jessell T. M. Developmental expression of the axonal glycoprotein TAG-1: differential regulation by central and peripheral neurons in vitro. Development. 1991 May;112(1):51–67. doi: 10.1242/dev.112.1.51. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Kidd G. J., Hauer P. E., Trapp B. D. Axons modulate myelin protein messenger RNA levels during central nervous system myelination in vivo. J Neurosci Res. 1990 Aug;26(4):409–418. doi: 10.1002/jnr.490260403. [DOI] [PubMed] [Google Scholar]
  36. Krantz D. E., Zipursky S. L. Drosophila chaoptin, a member of the leucine-rich repeat family, is a photoreceptor cell-specific adhesion molecule. EMBO J. 1990 Jun;9(6):1969–1977. doi: 10.1002/j.1460-2075.1990.tb08325.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kuchler S., Rougon G., Marschal P., Lehmann S., Reeber A., Vincendon G., Zanetta J. P. Location of a transiently expressed glycoprotein in developing cerebellum delineating its possible ontogenetic roles. Neuroscience. 1989;33(1):111–124. doi: 10.1016/0306-4522(89)90315-1. [DOI] [PubMed] [Google Scholar]
  38. Lehmann S., Kuchler S., Theveniau M., Vincendon G., Zanetta J. P. An endogenous lectin and one of its neuronal glycoprotein ligands are involved in contact guidance of neuron migration. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6455–6459. doi: 10.1073/pnas.87.16.6455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Letourneau P. C., Shattuck T. A., Roche F. K., Takeichi M., Lemmon V. Nerve growth cone migration onto Schwann cells involves the calcium-dependent adhesion molecule, N-cadherin. Dev Biol. 1990 Apr;138(2):430–442. doi: 10.1016/0012-1606(90)90209-2. [DOI] [PubMed] [Google Scholar]
  40. Lisanti M. P., Caras I. W., Davitz M. A., Rodriguez-Boulan E. A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J Cell Biol. 1989 Nov;109(5):2145–2156. doi: 10.1083/jcb.109.5.2145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lisanti M. P., Rodriguez-Boulan E. Glycophospholipid membrane anchoring provides clues to the mechanism of protein sorting in polarized epithelial cells. Trends Biochem Sci. 1990 Mar;15(3):113–118. doi: 10.1016/0968-0004(90)90195-h. [DOI] [PubMed] [Google Scholar]
  42. Lisanti M. P., Sargiacomo M., Graeve L., Saltiel A. R., Rodriguez-Boulan E. Polarized apical distribution of glycosyl-phosphatidylinositol-anchored proteins in a renal epithelial cell line. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9557–9561. doi: 10.1073/pnas.85.24.9557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Low M. G., Saltiel A. R. Structural and functional roles of glycosyl-phosphatidylinositol in membranes. Science. 1988 Jan 15;239(4837):268–275. doi: 10.1126/science.3276003. [DOI] [PubMed] [Google Scholar]
  44. Low M. G., Stiernberg J., Waneck G. L., Flavell R. A., Kincade P. W. Cell-specific heterogeneity in sensitivity of phosphatidylinositol-anchored membrane antigens to release by phospholipase C. J Immunol Methods. 1988 Oct 4;113(1):101–111. doi: 10.1016/0022-1759(88)90386-9. [DOI] [PubMed] [Google Scholar]
  45. Low M. G. The glycosyl-phosphatidylinositol anchor of membrane proteins. Biochim Biophys Acta. 1989 Dec 6;988(3):427–454. doi: 10.1016/0304-4157(89)90014-2. [DOI] [PubMed] [Google Scholar]
  46. Macklin W. B., Weill C. L., Deininger P. L. Expression of myelin proteolipid and basic protein mRNAs in cultured cells. J Neurosci Res. 1986;16(1):203–217. doi: 10.1002/jnr.490160118. [DOI] [PubMed] [Google Scholar]
  47. Mirsky R., Jessen K. R., Schachner M., Goridis C. Distribution of the adhesion molecules N-CAM and L1 on peripheral neurons and glia in adult rats. J Neurocytol. 1986 Dec;15(6):799–815. doi: 10.1007/BF01625196. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. Noda M., Yoon K., Rodan G. A., Koppel D. E. High lateral mobility of endogenous and transfected alkaline phosphatase: a phosphatidylinositol-anchored membrane protein. J Cell Biol. 1987 Oct;105(4):1671–1677. doi: 10.1083/jcb.105.4.1671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Persohn E., Pollerberg G. E., Schachner M. Immunoelectron-microscopic localization of the 180 kD component of the neural cell adhesion molecule N-CAM in postsynaptic membranes. J Comp Neurol. 1989 Oct 1;288(1):92–100. doi: 10.1002/cne.902880108. [DOI] [PubMed] [Google Scholar]
  51. Ploug M., Rønne E., Behrendt N., Jensen A. L., Blasi F., Danø K. Cellular receptor for urokinase plasminogen activator. Carboxyl-terminal processing and membrane anchoring by glycosyl-phosphatidylinositol. J Biol Chem. 1991 Jan 25;266(3):1926–1933. [PubMed] [Google Scholar]
  52. Powell S. K., Cunningham B. A., Edelman G. M., Rodriguez-Boulan E. Targeting of transmembrane and GPI-anchored forms of N-CAM to opposite domains of a polarized epithelial cell. Nature. 1991 Sep 5;353(6339):76–77. doi: 10.1038/353076a0. [DOI] [PubMed] [Google Scholar]
  53. Remahl S., Hilderbrand C. Relation between axons and oligodendroglial cells during initial myelination. I. The glial unit. J Neurocytol. 1990 Jun;19(3):313–328. doi: 10.1007/BF01188401. [DOI] [PubMed] [Google Scholar]
  54. Rothberg K. G., Ying Y. S., Kolhouse J. F., Kamen B. A., Anderson R. G. The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J Cell Biol. 1990 Mar;110(3):637–649. doi: 10.1083/jcb.110.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Roufa D., Bunge M. B., Johnson M. I., Cornbrooks C. J. Variation in content and function of non-neuronal cells in the outgrowth of sympathetic ganglia from embryos of differing age. J Neurosci. 1986 Mar;6(3):790–802. doi: 10.1523/JNEUROSCI.06-03-00790.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Salzer J. L., Bunge R. P., Glaser L. Studies of Schwann cell proliferation. III. Evidence for the surface localization of the neurite mitogen. J Cell Biol. 1980 Mar;84(3):767–778. doi: 10.1083/jcb.84.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Salzer J. L., Williams A. K., Glaser L., Bunge R. P. Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction. J Cell Biol. 1980 Mar;84(3):753–766. doi: 10.1083/jcb.84.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Schofield P. R., McFarland K. C., Hayflick J. S., Wilcox J. N., Cho T. M., Roy S., Lee N. M., Loh H. H., Seeburg P. H. Molecular characterization of a new immunoglobulin superfamily protein with potential roles in opioid binding and cell contact. EMBO J. 1989 Feb;8(2):489–495. doi: 10.1002/j.1460-2075.1989.tb03402.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Seeger M. A., Haffley L., Kaufman T. C. Characterization of amalgam: a member of the immunoglobulin superfamily from Drosophila. Cell. 1988 Nov 18;55(4):589–600. doi: 10.1016/0092-8674(88)90217-6. [DOI] [PubMed] [Google Scholar]
  60. Seilheimer B., Persohn E., Schachner M. Antibodies to the L1 adhesion molecule inhibit Schwann cell ensheathment of neurons in vitro. J Cell Biol. 1989 Dec;109(6 Pt 1):3095–3103. doi: 10.1083/jcb.109.6.3095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Selvaraj P., Rosse W. F., Silber R., Springer T. A. The major Fc receptor in blood has a phosphatidylinositol anchor and is deficient in paroxysmal nocturnal haemoglobinuria. Nature. 1988 Jun 9;333(6173):565–567. doi: 10.1038/333565a0. [DOI] [PubMed] [Google Scholar]
  62. Simmons D., Seed B. The Fc gamma receptor of natural killer cells is a phospholipid-linked membrane protein. Nature. 1988 Jun 9;333(6173):568–570. doi: 10.1038/333568a0. [DOI] [PubMed] [Google Scholar]
  63. Thompson J. A., Lau A. L., Cunningham D. D. Selective radiolabeling of cell surface proteins to a high specific activity. Biochemistry. 1987 Feb 10;26(3):743–750. doi: 10.1021/bi00377a014. [DOI] [PubMed] [Google Scholar]
  64. Toutant J. P., Richards M. K., Krall J. A., Rosenberry T. L. Molecular forms of acetylcholinesterase in two sublines of human erythroleukemia K562 cells. Sensitivity or resistance to phosphatidylinositol-specific phospholipase C and biosynthesis. Eur J Biochem. 1990 Jan 12;187(1):31–38. doi: 10.1111/j.1432-1033.1990.tb15274.x. [DOI] [PubMed] [Google Scholar]
  65. Towbin H., Staehelin T., Gordon J. 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):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Tse A. G., Barclay A. N., Watts A., Williams A. F. A glycophospholipid tail at the carboxyl terminus of the Thy-1 glycoprotein of neurons and thymocytes. Science. 1985 Nov 29;230(4729):1003–1008. doi: 10.1126/science.2865810. [DOI] [PubMed] [Google Scholar]
  67. Voyvodic J. T. Target size regulates calibre and myelination of sympathetic axons. Nature. 1989 Nov 23;342(6248):430–433. doi: 10.1038/342430a0. [DOI] [PubMed] [Google Scholar]
  68. Webster H. D., Martin R., O'Connell M. F. The relationships between interphase Schwann cells and axons before myelination: a quantitative electron microscopic study. Dev Biol. 1973 Jun;32(2):401–416. doi: 10.1016/0012-1606(73)90250-9. [DOI] [PubMed] [Google Scholar]
  69. Weinberg H. J., Spencer P. S. Studies on the control of myelinogenesis. II. Evidence for neuronal regulation of myelin production. Brain Res. 1976 Aug 27;113(2):363–378. doi: 10.1016/0006-8993(76)90947-1. [DOI] [PubMed] [Google Scholar]
  70. Wood P. M., Bunge R. P. Evidence that sensory axons are mitogenic for Schwann cells. Nature. 1975 Aug 21;256(5519):662–664. doi: 10.1038/256662a0. [DOI] [PubMed] [Google Scholar]
  71. Wood P. M., Schachner M., Bunge R. P. Inhibition of Schwann cell myelination in vitro by antibody to the L1 adhesion molecule. J Neurosci. 1990 Nov;10(11):3635–3645. doi: 10.1523/JNEUROSCI.10-11-03635.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wood P. M., Williams A. K. Oligodendrocyte proliferation and CNS myelination in cultures containing dissociated embryonic neuroglia and dorsal root ganglion neurons. Brain Res. 1984 Feb;314(2):225–241. doi: 10.1016/0165-3806(84)90045-2. [DOI] [PubMed] [Google Scholar]
  73. Xue G. P., Rivero B. P., Morris R. J. The surface glycoprotein Thy-1 is excluded from growing axons during development: a study of the expression of Thy-1 during axogenesis in hippocampus and hindbrain. Development. 1991 May;112(1):161–176. doi: 10.1242/dev.112.1.161. [DOI] [PubMed] [Google Scholar]

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