Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS

Nature Reviews Neuroscience

Volumn 4, Issue 9, 2003, Pages 703-713

  Filbin, Marie T ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH INHIBITOR; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN;

ANIMAL; CENTRAL NERVOUS SYSTEM; CHEMISTRY; HUMAN; METABOLISM; MYELIN SHEATH; NERVE FIBER; NERVE REGENERATION; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; BRAIN INJURY; MAMMAL; MOUSE; NERVE FIBER REGENERATION; NERVOUS SYSTEM INJURY; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD INJURY;

ANIMALS; AXONS; CENTRAL NERVOUS SYSTEM; GROWTH INHIBITORS; HUMANS; MYELIN SHEATH; MYELIN-ASSOCIATED GLYCOPROTEIN; NERVE REGENERATION; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 0141499228     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn1195     Document Type: Article

References (108)

1. Fitch, M. T & Silver, J. in CNS Regeneration (eds Tuszynski, M. H. & Kordower, J. H.) 55-88 (Academic, San Diego, 1999).
2. Qiu, J., Cai, D. & Filbin, M. T. Glial inhibition of nerve regeneration in the mature mammalian CNS. Glia 29, 166-174 (2000).
3. Schwab, M. E. & Bartholdi, D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319-370 (1996).
4. Huang, D. W., McKerracher, L., Braun, P. E. & David, S. A therapeutic vaccine approach to stimulate axon regeneration in the adult mammalian spinal cord. Neuron 24, 639-647 (1999).
5. Ramon y Cajal, S. Cajal's Degeneration & Regeneration of the Nervous System (eds DeFelipe, J. & Jones, E. G.) (Oxford Univ. Press, Oxford, 1928).
6. Berry, M. Post-injury myelin-breakdown products inhibit axonal growth: an hypothesis to explain the failure of axonal regeneration in the mammalian central nervous system. Bibl. Anat. 23, 1-11 (1982).
7. Crutcher, K. A. Tissue sections from the mature rat brain and spinal cord as substrates for neurite outgrowth in vitro: extensive growth on gray matter but little growth on white matter Exp. Neurol. 104, 39-54 (1989).
8. Caroni, P. & Schwab, M. E. Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J. Cell Biol. 106, 1281-1288 (1988).
9. Caroni, P. & Schwab, M. E. Antibody against myelin- associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1, 85-96 (1988).
10. Schnell, L. & Schwab, M. E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-asso- ciated neurite growth inhibitors. Nature 343, 269-272 (1990).
11. Chen, M. S. et al. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403, 434-439 (2000).
12. GrandPre, T, Nakamura, F., Vartanian, T. & Strittmatter, S. M. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 403, 439-444 (2000).
13. Prinjha, R. et al. Inhibitor of neurite outgrowth in humans. Nature 403, 383-384 (2000).
14. Huber, A. B., Weinmann, O., Brosamle, C., Oertle, T. & Schwab, M. E. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J. Neurosci. 22, 3553-3567 (2002).
15. Wang, X. et al. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 22, 5505-15 (2002).
16. McKerracher, L. et al. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13, 805-811 (1994).
17. Mukhopadhyay, G., Doherty, P, Walsh, F. S., Crocker, P. R. & Filbin, M. T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13, 757-767 (1994).
18. Cai, D. et al. Neuronal cyclic amp controls the developmental loss in ability of axons to regenerate. J. Neurosci. 21, 4731-4739 (2001).
19. de Bellard, M. & Filbin, M. T. Myelin-associated glycoprotein, MAG, selectively binds several neuronal proteins. J. Neurosci. Res. 56, 213-218 (1999).
20. Turnley, A. M. & Bartlett, P. F. MAG and MOG enhance neurite outgrowth of embryonic mouse spinal cord neurons. Neuroreport 9, 1987-1990 (1998).
21. Johnson, P. W. et al. Recombinant myelin-associated glycoprotein confers neural adhesion and neurite outgrowth function. Neuron 3, 377-385 (1989).
22. Salzer, J. L., Holmes, W. P & Colman, D. R. The amino acid sequences of the myelin-associated glycoproteins: homology to the immunoglobulin gene superfamily. J. Cell Biol. 104, 957-965 (1987).
23. Salzer, J. L. et al. Structure and function of the myelin- associated glycoproteins. Ann. NY Acad. Sci. 605, 302-312 (1990).
24. Kelm, S. et al. 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 (1994).
25. Tang, S. et al. Myelin-associated glycoprotein interacts with neurons via a sialic acid binding site at ARG118 and a distinct neurite inhibition site. J. Cell Biol. 138, 1355-1366 (1997).
26. Trapp, B. D. Distribution of the myelin-associated glycoprotein and P0 protein during myelin compaction in quaking mouse peripheral nerve. J. Cell Biol. 107, 675-685 (1988).
27. Willison, H. J. et al. Myelin-associated glycoprotein and related glycoconjugates in developing cat peripheral nerve: a correlative biochemical and morphometric study. J. Neurochem. 49, 1853-1862 (1987).
28. Wang, K. C. et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417, 941-944 (2002).
29. Habib, A. A. et al. Expression of the oligodendrocyte-myelin glycoprotein by neurons in the mouse central nervous system. J. Neurochem. 70, 1704-1711 (1998).
30. Mikol, D. D., Gulcher, J. R. & Stefansson, K. The oligodendrocyte-myelin glycoprotein belongs to a distinct family of proteins and contains the HNK-1 carbohydrate. J. Cell Biol. 110, 471-479 (1990).
31. Kottis, V. et al. Oligodendrocyte-myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. J. Neurochem. 82, 1566-1569 (2002).
32. Fournier, A. E., GrandPre, T. & Strittmatter, S. M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341-346 (2001).
33. Josephson, A. et al. Nogo-receptor gene activity: cellular localization and developmental regulation of mRNA in mice and humans. J. Comp. Neurol. 453, 292-304 (2002).
34. Oertle, T. et al. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J. Neurosci. 23, 5393-5406 (2003).
35. Liu, B. P, Fournier, A., GrandPre, T. & Strittmatter, S. M. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 297, 1190-1193 (2002).
36. Domeniconi, M. et al. Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35, 283-290 (2002).
37. Yamashita, T., Higuchi, H. & Tohyama, M. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 157, 565-570 (2002).
38. Wang, K. C., Kim, J. A., Sivasankaran, R., Segal, R. & He, Z. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74-78 (2002).
39. NTR and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nature Neurosci. 5, 1302-1308 (2002).
40. He, X. L. et al. Structure of the Nogo receptor ectodomain. A recognition module implicated in myelin inhibition. Neuron 38, 177-185 (2003).
41. Bartsch, U. et al. Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron 15, 1375-1381 (1995).
42. Li, M. et al. Myelin-associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse. J. Neurosci. Res. 46, 404-414 (1996).
43. Bregman, B. S. et al. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378, 498-501 (1995).
44. Schnell, L. & Schwab, M. E. Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur. J. Neurosci. 5, 1156-1171 (1993).
45. GrandPre, T., Li, S. & Strittmatter, S. M. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417, 547-551 (2002).
46. Kim, J. E., Li, S., GrandPre, T., Qiu, D. & Strittmatter, S. M. Axon regeneration in young adult mice lacking nogo-a/b. Neuron 38, 187-199 (2003).
47. Simonen, M. et al. Systemic deletion of the myelin- associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38, 201-211 (2003).
48. Zheng, B. et al. Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 38, 213-224 (2003).
49. Trapp, B. D. Myelin-associated glycoprotein. Location and potential functions. Ann. NY Acad. Sci. 605, 29-43 (1990).
50. Apostolski, S. et al. Identification of Gal(p1 -3)GalNAc bearing glycoproteins at the nodes of Ranvier in peripheral nerve. J. Neurosci. Res. 38, 134-141 (1994).
51. Josephson, A., Widenfalk, J., Widmer, H. W., Olson, L. & Spenger, C. NOGO mRNA expression in adult and fetal human and rat nervous tissue and in weight drop injury. Exp. Neurol. 169, 319-328 (2001).
52. McMahon, S. B., Armanini, M. P., Ling, L. H. & Phillips, H. S. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12, 1161-1171 (1994).
53. Wright, D. E. & Snider, W. D. Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. J. Comp. Neurol. 351, 329-338 (1995).
54. Ernfors, P., Henschen, A., Olson, L. & Persson, H. Expression of nerve growth factor receptor mRNA is developmentally regulated and increased after axotomy in rat spinal cord motoneurons. Neuron 2, 1605-1613 (1989).
55. Koliatsos, V. E., Crawford, T. O. & Price, D. L. Axotomy induces nerve growth factor receptor immunoreactivity in spinal motor neurons. Brain Res. 549, 297-304 (1991).
56. Walsh, G. S., Krol, K. M., Crutcher, K. A. & Kawaja, M. D. Enhanced neurotrophin-induced axon growth in myelinated portions of the CNS in mice lacking the p75 neurotrophin receptor. J. Neurosci. 19, 4155-4168 (1999).
57. Davies, S. J. et al. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390, 680-683 (1997).
58. Davies, S. J., Goucher, D. R., Doller, C. & Silver, J. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 19, 5810-5822 (1999).
59. Lehmann, M. et al. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J. Neurosci. 19, 7537-7547 (1999).
60. Hall, A. Rho GTPases and the actin cytoskeleton. Science 279, 509-514 (1998).
61. Jin, Z. & Strittmatter, S. M. Rac1 mediates collapsin-1- induced growth cone collapse. J. Neurosci. 17, 6256-6263 (1997).
62. Fournier, A. E., Takizawa, B. T. & Strittmatter, S. M. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci. 23, 1416-1423 (2003).
63. Niederost, B., Oertle, T., Fritsche, J., McKinney, R. A. & Bandtlow, C. E. Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J. Neurosci. 22, 10368-10376 (2002).
64. Vinson, M. et al. Myelin-associated glycoprotein interacts with ganglioside GT1b. A mechanism for neurite outgrowth inhibition. J. Biol. Chem. 276, 20280-20285 (2001).
65. Yamashita, T. & Tohyama, M. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nature Neurosci. 6, 461-467 (2003).
66. Dergham, P. et al. Rho signaling pathway targeted to promote spinal cord repair. J. Neurosci. 22, 6570-6577 (2002).
67. Igarashi, M., Strittmatter, S. M., Vartanian, T. & Fishman, M. C. Mediation by G proteins of signals that cause collapse of growth cones. Science 259, 77-79 (1993).
68. Cai, D., Shen, Y., de Bellard, M., Tang, S. & Filbin, M. T. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22, 89-101 (1999).
69. Bandtlow, C. E., Schmidt, M. F., Hassinger, T. D., Schwab, M. E. & Kater, S. B. Role of intracellular calcium in NI-35- evoked collapse of neuronal growth cones. Science 259, 80-83 (1993).
70. NTR. Curr. Opin. Neurobiol. 12, 260-267 (2002).
71. Fournier, A. E., Gould, G. C., Liu, B. P. & Strittmatter, S. M. Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. J. Neurosci. 22, 8876-8883 (2002).
72. Winton, M. J., Dubreuil, C. I., Lasko, D., Leclerc, N. & McKerracher, L. Characterization of new cell permeable C3- like proteins that inactivate Rho and stimulate neurite outgrowth on inhibitory substrates. J. Biol. Chem. 277, 32820-32829 (2002).
73. Bandtlow, C. E. Regeneration in the central nervous system. Exp. Gerontol. 38, 79-86 (2003).
74. Song, H. et al. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281, 1515-1518 (1998).
75. Ramer, M. S., Priestley, J. V. & McMahon, S. B. Functional regeneration of sensory axons into the adult spinal cord. Nature 403, 312-316 (2000).
76. Qiu, J. et al. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 895-903 (2002).
77. Cai, D. et al. Arginase I and polyamines are downstream from cyclic AMP in the pathway that overcomes inhibition of axonal regeneration by Mag and myelin in vitro. Neuron 35, 711-719 (2002).
78. Chu, P. J., Saito, H. & Abe, K. Polyamines promote regeneration of injured axons of cultured rat hippocampal neurons. Brain Res. 673, 233-241 (1995).
79. Dornay, M., Gilad, V. H., Shiler, I. & Gilad, G. M. Early polyamine treatment accelerates regeneration of rat sympathetic neurons. Exp. Neurol. 92, 665-674 (1986).
80. Kauppila, T., Stenberg, D. & Porkka-Heiskanen, T. Putative stimulants for functional recovery after neural trauma: only spermine was effective. Exp. Neurol. 99, 50-58 (1988).
81. Banan, A., McCormack, S. A. & Johnson, L. R. Polyamines are required for microtubule formation during gastric mucosal healing. Am. J. Physiol. 274, G879-885 (1998).
82. Kaminska, B., Kaczmarek, L. & Grzelakowska-Sztabert, B. Inhibitors of polyamine biosynthesis affect the expression of genes encoding cytoskeletal proteins. FEBS Lett. 304, 198-200 (1992).
83. Wolff, J. Promotion of microtubule assembly by oligocations: cooperativity between charged groups. Biochemistry 37, 10722-10729 (1998).
84. Williams, K. Interactions of polyamines with ion channels. Biochem. J. 325, 289-297 (1997).
85. Chao, J. et al. N1-dansyl-spermine and N1-(noctanesulfonyl)-spermine, novel glutamate receptor antagonists: block and permeation of N-methyl-D-aspartate receptors. Mol. Pharmacol. 51, 861–871 (1997).
86. Kashiwagi, K., Pahk, A. J., Masuko, T, Igarashi, K. & Williams, K. Block and modulation of N-methyl-D-aspartate receptors by polyamines and protons: role of amino acid residues in the transmembrane and pore-forming regions of NR1 and NR2 subunits. Mol. Pharmacol. 52, 701-713 (1997).
87. Williams, K., Zappia, A. M., Pritchett, D. B., Shen, Y. M. & Molinoff, P B. Sensitivity of the N-methyl-D-aspartate receptor to polyamines is controlled by NR2 subunits. Mol. Pharmacol. 45, 803-809 (1994).
88. Cohen, S. (ed.) A Guide to the Polyamines (Oxford Univ. Press, New York, 1998).
89. Aizenman, C. D., Munoz-Elias, G. & Cline, H. T. Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines. Neuron 34, 623-634 (2002).
90. Ming, G., Henley, J., Tessier-Lavigne, M., Song, H. & Poo, M. Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29, 441-452 (2001).
91. Bregman, B. S. & Goldberger, M. E. Anatomical plasticity and sparing of function after spinal cord damage in neonatal cats. Science 217, 553-555 (1982).
92. Kunkel-Bagden, E., Dai, H. N. & Bregman, B. S. Recovery of function after spinal cord hemisection in newborn and adult rats: differential effects on reflex and locomotor function. Exp. Neurol. 116, 40-51 (1992).
93. Neumann, S. & Woolf, C. J. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23, 83-91 (1999).
94. Richardson, P. M. & Issa, V. M. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309, 791-793 (1984).
95. DeBellard, M. E., Tang, S., Mukhopadhyay, G., Shen, Y. J. & Filbin, M. T. Myelin-associated glycoprotein inhibits axonal regeneration from a variety of neurons via interaction with a sialoglycoprotein. Mol. Cell. Neurosci. 7, 89-101 (1996).
96. Neumann, S., Bradke, F., Tessier-Lavigne, M. & Basbaum, A. I. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885-893 (2002).
97. Bonilla, I. E., Tanabe, K. & Strittmatter, S. M. Small proline- rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J. Neurosci. 22, 1303-1315 (2002).
98. Schreyer, D. J. & Skene, J. H. Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: delayed accumulation and correlation with regenerative potential. J. Neurosci. 11, 3738-3751 (1991).
99. Schreyer, D. J. & Skene, J. H. Injury-associated induction of GAP-43 expression displays axon branch specificity in rat dorsal root ganglion neurons. J. Neurobiol. 24, 959-970 (1993).
100. Bomze, H. M., Bulsara, K. R., Iskandar, B. J., Caroni, P. & Skene, J. H. Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nature Neurosci. 4, 38-43 (2001).
101. Scherer, S. S. & Salzer, J. L. in Glial Cell Development; Basic Principles and Clinical Relevance (eds Jessen, K. R. & Richardson, W. D.) 165-185 (Bios Scientific Publishers, Oxford, 1996).
102. Rapalino, O. et al. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nature Med. 4, 814-821 (1998).
103. Leskovar, A., Moriarty, L. J., Turek, J. J., Schoenlein, I. A. & Borgens, R. B. The macrophage in acute neural injury: changes in cell numbers over time and levels of cytokine production in mammalian central and peripheral nervous systems. J. Exp. Biol. 203, 1783-1795 (2000).
104. Kelm, S. et al. Functional groups of sialic acids involved in binding to siglecs (sialoadhesins) deduced from interactions with synthetic analogues. Eur. J. Biochem. 255, 663-672 (1998).
105. Collins, B. E. et al. Sialic acid specificity of myelin-associated glycoprotein binding. J. Biol. Chem. 272, 1248-1255 (1997).
106. Vyas, A. A. et al. Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proc. Natl Acad. Sci. USA 99, 8412-8417 (2002).
107. Yang, L. J. et al. Gangliosides are neuronal ligands for myelin-associated glycoprotein. Proc. Natl Acad. Sci. USA 93, 814-818 (1996).
108. Bandtlow, C. E. & Loschinger, J. Developmental changes in neuronal responsiveness to the CNS myelin-associated neurite growth inhibitor NI-35/250. Eur. J. Neurosci. 9, 2743-2752 (1997).