Myelin-associated glycoprotein inhibits axonal regeneration from a variety of neurons via interaction with a sialoglycoprotein

Molecular and Cellular Neurosciences

Volumn 7, Issue 2, 1996, Pages 89-101

  DeBellard, Maria Elena ^a   Tang, Song ^a   Mukhopadhyay, Gitali ^a   Shen, Ying Jing ^a   Filbin, Marie T ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN ASSOCIATED GLYCOPROTEIN; SIALOGLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DEVELOPMENT; GENETIC TRANSFECTION; HAMSTER; HIPPOCAMPUS; NERVE GROWTH; NERVE REGENERATION; NEWBORN; NONHUMAN; OVARY CELL; PRIORITY JOURNAL; RAT; RETINA; SPINAL GANGLION; SUPERIOR CERVICAL GANGLION;

EID: 0029993455     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1996.0007     Document Type: Article

References (71)

1. Bartsch, L., Bandtlow, C. E., Schnell, L., Bartsch, S., Spillmann, A. A., Rubin, B. P., Hillenbrand, R., Montag, D., Schwab, M. E., and Schachner, M. (1995). Lack of evidence that the myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron 15: 1375-1381.
2. Berry, M. (1982). Post-injury myelin-breakdown products inhibit axonal growth: An hypothesis to explain the failure of axonal regeration in the mammalian central nervous system. Bibl. Anat. 23: 1-11.
3. Bixby, J. L., and Harris, W. A. (1991). Molecular mechanisms of axonal growth and guidance. Annu. Rev. Cell Biol. 7: 117-159.
4. Bregman, B. S., Kunke-Bagden, E., Schnell, L., Dal, H. N., Gao, D., and Schwab, M. E. (1995). Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378: 498-501.
5. Brown, M. C., Perry, V. H., Lunn, E. R., Gordon, S., and Heumann, R. (1991). Macrophage dependence of peripheral sensory nerve regeneration: Possible involvement of nerve growth. Neuron 6: 359-370.
6. Brown, M. C., Lunn, E. R., and Perry, V. H. (1992). Consequences of slow Wallerian degeneration for regenerating motor and sensory axons. J. Neurobiol. 23: 521-536.
7. Cajal, S. R. Y. (1928). Degeneration and Regeneration of the Nervous System. Oxford University Press, London. Translated by R. M. May.
8. Carbonetto, S., Evans, D., and Cochart, P. (1987). Nerve fiber growth in culture in tissue substrates from central and peripheral nervous system. J. Neurosci. 7: 610-620.
9. Caroni, P., and Schwab, M. E. (1988a). Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1: 85-96.
10. Caroni, P., and Schwab, M. E. (1988b). Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J. Cell Biol. 106: 1281-1288.
11. Chiquet, M. (1989). Neurite growth inhibition by CNS myelin proteins: A mechanism to confine fiber tracts? Trends Neurosci. 12: 1-3.
12. Colamarino, S. A., and Tessier-Lavigne, M. (1995). The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81: 621-629.
13. Colello, R. J., and Schwab, M. E. (1994). A role for oligodendrocytes in the stabilization of optic axon numbers. J. Neurosci. 14: 6446-6452.
14. Crocker, P. R., and Kelm, S. (1996). Methods for studying the cellular binding properties of lectin-like receptors. In Handbook of Experimental Immunology, in press.
15. Crocker, P. R., Mucklow, S., Bouckson, V., McWilliam, A., Willis, A. C., Gordon, S., Milon, G., Kelm, S., and Bradfield, P. (1994). Sialoadhesin, a macrophage sialic acid-binding receptor for haemopoietic cells with 17 immunoglobulin-like domains. EMBO J. 13: 65-74.
16. Crocker, P. R., Kelm, S., Dubois, C., Martin, B., McWilliam, A. S., Shotton, D. M., Paulson, J. C., and Gordon, S. (1991). Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages. EMBO J. 10: 1661-1669.
17. Crutcher, K. A. (1989). Tissue sections from mature rat brain and spinal cord as substrates for neurite outgrowths in vitro: Extensive growth on gray matter but little on white matter. Exp. Neurol. 104: 39-54.
18. David, S., and Aguayo, A. J. (1981). Axonal elongation into peripheral nervous system 'bridges' after central nervous system injury in adult rats. Science 214: 931-933.
19. Doherty, P., and Walsh, F. S. (1989). Neurite guidance molecules. Curr. Opin. Cell Biol. 1: 1102-1106.
20. Doherty, P., Fruns, M., Seaton, P., Dickson, G., Barton, C. H., Sears, T. A., and Walsh, F. S. (1990a). A threshold effect of the major isoforms of N CAM on neurite outgrowth. Nature 343: 464-466.
21. Doherty, P., Cohen, J., and Walsh, F. S. (1990b). Neurite outgrowth in response to transfected N CAM changes during development and is modulated by polysialic acid. Neuron 5: 209-219.
22. Drescher, U., Kremoser, C., Handwerker, C., Loschinger, J., Noda, M., and Bonhoeffer, F. (1995). In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82: 359-370.
23. Fawcett, J. W., and Keynes, R. J. (1990). Peripheral nerve regeneration. Annu. Rev. Neurosci. 13: 43-60.
24. Filbin, M. T. (1995). Myelin-associated glycoprotein: A role in myelination and in the inhibition of axonal regeneration? Curr. Opin. Neurobiol. 5: 588-595.
25. Filbin, M. T., and Tennekoon, G. I. (1990). High level of expression of the myelin protein Po in Chinese hamster ovary cells. J. Neurochem. 55: 500-505.
26. Filbin, M. T., Walsh, F. S., Trapp, B. D., Pizzey, J. A., and Tennekoon, G. I. (1990). Role of myelin Po-protein as a homophilic adhesion molecule. Nature 344: 871-872.
27. Freeman, S. D., Kelm, S., Barber, E. K., and Crocker, P. R. (1995). Characterisation of CD33 as a new member of the Sialoadhesin family of cellular interactions molecules. Blood 85: 2005-2012.
28. Fruttiger, M., Montag, D., Schachner, M., and Martini, R. (1995). Crucial role for the myelin-associated glycoprotein in the maintenance of axonal-myelin integrity. Eur. J. Neurosci. 7: 511-515.
29. Johnson, A. R. (1993). Contact inhibition in the failure of mammalian CNS axonal regeneration. BioEssays 15: 807-813.
30. Johnson, P. W., Abramow-Newerly, W., Seilheimer, B., Sadoul, R., Tropak, M. B., Arquint, M., Dunn, R. J., Schachner, M., and Roder, J. C. (1989). Recombinant myelin associated glycoprotein confers neural adhesion and neurite outgrowth function. Neuron 3: 377-385.
31. Kapfhammer, J. P., and Schwab, M. E. (1994). Inverse patterns of myelination and GAP-43 expression in the adult CNS: Neurite growth inhibitors as regulators of neuronal plasticity? J. Comp. Neurol 340: 194-206.
32. Kelm, S., Pelz, A., Schauer, R., Filbin, M. T., Tang, S., de Bellard, M-E., Schnaar, R. L., Mahoney, J. A., Hartnell, A., Bradfield, P., and Crocker, P. R. (1994). Sialoadhesin, myelin-associated glycoprotein and CD22 define a new family of sialic acid-dependent adhesion molecules of the immunoglobulin superfamily. Curr. Biol. 4: 965-972.
33. Kennedy, T., Serafini, T., de la Torre, J. R., and Tessier-Lavigne, M. (1994). Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78: 425-435.
34. Keynes, R. J., and Cook, G. M. W. (1995). Repulsive and inhibitory signals. Curr. Opin. Neurobiol. 5: 75-82.
35. Kleitman, N., Wood, P. M., and Bunge, R. P. (1991). In Culturing Nerve Cells (G. Banker and K. Goslin, Eds.), pp. 337-378. MIT Press, Cambridge, MA/London, England.
36. Lee, S. J., and Nathans, D. (1988). Proliferin secreted by cultured cells binds to mannose-6-phosphate receptors. J. Biol. Chem. 263: 3521-3527.
37. Li, C., Tropak, M. B., Gerlai, R., Clapoff, S., Abramow-Newerly, W., Trapp, B., Peterson, A., and Roder, J. (1994). Myelination in the absence of myelin-associated glycoprotein. Nature 369: 747-750.
38. Luo, Y., Raible, D., and Raper, J. A. (1993). Collapsin: A protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75: 217-227.
39. Luo, Y., Shepherd, I., Li, J., Renzi, M. J., Chang, S., and Raper, J. A. (1995). A family of molecules related to collapsin in the embryonic chick nervous system. Neuron 14: 1131-1140.
40. Martini, R., and Schachner, M. (1986). Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve. J. Cell Biol. 103: 2439-2448.
41. Matthes, D. J., Sink, H., Kolodkin, A. L., and Goodman, C. S. (1995). Semaphorin II can function as a selective inhibitor of specific synaptic arborizations. Cell 81: 631-639.
42. McKerracher, L., David, S., Jackson, D. L., Kottis, V., Dunn, R. J., and Braun, P. E. (1994). Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite outgrowth. Neuron 13: 805-811.
43. Messersmith, E. K., Leonardo, E. D., Shatz, C. J., Tessier-Lavigne, M., Goodman, C., and Kolodkin, A. L. (1995). Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron 14: 949-959.
44. Montag, D., Giese, K. P., Bartsch, U., Martini, R., Lang, Y., Bluthmann, H., Karthigasan, J., Kirschner, D. A., Wintergerst, E. S., Nave, K. A., Zielasek, J., Toyka, K., Lipp, H. P., and Schachner, M. (1994). Mice deficient for the myelin-associated glycoprotein show subtle abnormalities in myelin. Neuron 13: 229-246.
45. Mukhopadhyay, G., Doherty, P., Walsh, F. S., Crocker, P. R., and Filbin, M. T. (1994). A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13: 757-767.
46. Owens, G. C., and Bunge, R. P. (1991). Schwann cells infected with a recombinant retrovirus expressing myelin-associated glycoprotein antisense RNA do not form myelin. Neuron 7: 565-575.
47. Owens, G. C., Boyd, C. J., Bunge, R. P., and Salzer, J. L. (1990). Expression of recombinant myelin-associated glycoprotein in primary Schwann cells promotes the initial investment of axons by myelinating Schwann cells. J. Cell Biol. 111: 1171-1182.
48. Poltorak, M., Sadoul, R., Keilhauer, G., Landa, C., Fahrig, T., and Schachner, M. (1987). Myelin-associated glycoprotein, a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte interaction. J. Cell Biol. 105: 1893-1899.
49. Powell, L. D., and Varki, A. (1995). I-type lectins: Carbohydrate-binding proteins of the immunoglobulin superfamily. J. Biol. Chem. 270: 14243-14246.
50. Powell, L. D., Jain, R. K., Matta, K. L., Sabesan, S., and Varki, A. (1995). Characterization of sialooligosaccharide binding by recombinant soluble and native cell-associated CD22. J. Biol. Chem. 270: 7523-7532.
51. Puschel, A. W., Adams, R. H., and Betz, H. (1995). Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 14: 941-948.
52. Quarles, R. H. (1984). Myelin-associated glycoprotein in development and disease. Dev. Neurosci. 6: 285-303.
53. Sako, D., Comess, K. M., Barone, K. M., Camphausen, R. T., Cumming, D. A., and Shaw, G. D. (1995). A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell 83: 323-331.
54. Salzer, J. L., Holmes, W. P., and Colman, D. R. (1987). The amino acid sequences of the myelin-associated glycoproteins: Homology to the immunoglobulin gene superfamiy. J. Cell Biol. 104: 957-865.
55. Salzer, J. L., Pedraza, L., Brown, M., Struyk, A., Afar, D., and Bell, J. (1990). Structure and function of the myelin-associated glycoproteins. Ann. N.Y. Acad. Sci. 605: 29-43.
56. Savio, T., and Schwab, M. E. (1989). Rat CNS white matter, but not gray matter, is non-permissive for neuronal cell adhesion and fiber outgrowth. J. Neurosci. 9: 1126-1133.
57. Schafer, M., Fruttiger, M., Montag, D., Schachner, M., and Martini, R. (1995). Disruption of the myelin-associated glycoprotein gene improves regeneration in C57BL/Wld mice. Soc. Neurosci. 612: 1.
58. Schnell, L., and Schwab, M. E. (1990). Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343: 269-272.
59. Schwab, M. E., and Caroni, P. (1988). Oligodendrocytes and CNS myelin are non-permissive substrates for neurite outgrowth and fibroblast spreading in vitro. J. Neurosci. 8: 2381-2391.
60. Schwab, M. E., Kapfhammer, J. P., and Bandtlow, C. E. (1993). Inhibitors of neurite growth. Annu. Rev. Neurosci. 16: 565-596.
61. Schwegler, G., Schwab, M. E., and Kapfhammer, J. P. (1995). Increased collateral sprouting of primary afferents in the myelin-free spinal cord. J. Neurosci. 15: 2756-2767.
62. Serafini, T., Kennedy, T., Galko, M., Mirzyan, C., Jessell, T., and Tessier-Lavigne, M. (1994). The Netrins define a family of axon outgrowth-promoting proteins with homology to C. elegans UNC-6. Cell 78: 409-424.
63. Stamenkovic, I., Sgroi, D., Aruffo, A., Sy, M. S., and Anderson, T. (1991). The lymophocyte-B adhesion molecule CD22 interacts with leukocyte common antigen CD45RO on T-cells and α-2,6 sialyltransferase, CD75, on B-cells. Cell 66: 1133-1144.
64. Timsit, S., Martinez, S., Allinquant, B., Peyron, F., Puelles, L., and Zalc, B. (1995). Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J. Neurosci. 15: 1012-1024.
65. Trapp, B. D., Andrews, S. B., Cootauco, C., and Quarles, R. H. (1989). The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes. J. Cell Biol. 109: 2417-2426.
66. Trapp, B. D. (1990). Myelin associated glycoprotein, location and potential function. Ann. N.Y. Acad. Sci. 605: 29-43.
67. Trapp, B. D., and Quarles, R. H. (1984). Immunocytochemical localization of the myelin-associated glycoprotein, fact or antifact? J. Neuroimmunol. 6: 231-249.
68. Urlaub, G., and Chasin, L. A. (1980). Isolation of Chinese hamster cell mutants deficient in dihydrofolate reductase activity. Proc. Natl. Acad. Sci. USA 77: 4216-4220.
69. Watanabe, E., and Murakami, F. (1990). Cell attachment to and neurite outgrowth on tissue sections of developing, mature and lesioned brain: The role of inhibitory factors in CNS white matter. Neurosci. Res. 8: 83-99.
70. Weinberg, E. L., and Spencer, P. S. (1979). Studies on the control of myelingenesis. 3. Signaling of oligodendrocyte myelination by regenerating peripheral axons. Brain Res. 162: 273-279.
71. Yu, W. P., Collarini, E. J., Pringle, N. P., and Richardson, W. D. (1994). Embryonic expression of myelin genes: Evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron 12: 1353-1362.