Myelin associated inhibitors: A link between injury-induced and experience-dependent plasticity

Experimental Neurology

Volumn 235, Issue 1, 2012, Pages 43-52

  Akbik, Feras ^a   Cafferty, William B J ^a   Strittmatter, Stephen M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activity dependent plasticity; Axons; Experience dependent plasticity; MAG; Myelin; Nogo; Nogo Receptor 1; OMgp; PirB; Plasticity; Regeneration; Spinal cord injury; Stroke

Indexed keywords

EPHRIN; IN 1; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; MYELIN; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN ASSOCIATED INHIBITOR; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NEP 1 40; NEUROTROPHIN RECEPTOR P75; NOGO 66 RECEPTOR 1; NOGO A ANTIBODY; PAIRED IMMUNOGLOBULIN LIKE RECEPTOR B; PEPTIDE DERIVATIVE; PLEXIN; PROTEIN NOGO A; PROTEOCHONDROITIN SULFATE; SEMAPHORIN; UNCLASSIFIED DRUG;

CYTOSKELETON; DRUG EFFECT; EXPERIENCE; HUMAN; INTRACELLULAR SIGNALING; LEARNING; MEMORY; MYELINATION; NERVE CELL PLASTICITY; NERVE FIBER REGENERATION; NERVE REGENERATION; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SPINAL CORD INJURY;

ANIMALS; AXONS; BRAIN; GPI-LINKED PROTEINS; MYELIN PROTEINS; MYELIN-ASSOCIATED GLYCOPROTEIN; NEURONAL PLASTICITY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84859899331     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.06.006     Document Type: Review

References (110)

1. Atwal J.K., et al. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322(5903):967-970.
2. Bandtlow C., Zachleder T., Schwab M. Oligodendrocytes arrest neurite growth by contact inhibition. J. Neurosci. 1990, 10(12):3837-3848.
3. Bareyre F.M., et al. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 2004, 7(3):269-277.
4. Barton W.A., et al. Structure and axon outgrowth inhibitor binding of the Nogo-66 receptor and related proteins. EMBO J. 2003, 22(13):3291-3302.
5. Bartsch U., Kirchhoff F., Schachner M. Immunohistological localization of the adhesion molecules L1, N-CAM, and MAG in the developing and adult optic nerve of mice. J. Comp. Neurol. 1989, 284(3):451-462.
6. Bartsch U., et al. Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron 1995, 15(6):1375-1381.
7. Bradbury E.J., et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416(6881):636-640.
8. Bregman B.S., et al. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 1995, 378(6556):498-501.
9. Brosamle C., et al. Regeneration of lesioned corticospinal tract fibers in the adult rat induced by a recombinant, humanized IN-1 antibody fragment. J. Neurosci. 2000, 20(21):8061-8068.
10. Budel S., et al. Genetic variants of Nogo-66 receptor with possible association to schizophrenia block myelin inhibition of axon growth. J. Neurosci. 2008, 28(49):13161-13172.
11. Budel S., et al. Genetic variants of Nogo-66 Receptor with possible association to schizophrenia block myelin inhibition of axon growth. J. Neurosci. 2008, 28(49):13161-13172.
12. Buffo A., et al. Application of neutralizing antibodies against NI-35/250 myelin-associated neurite growth inhibitory proteins to the adult rat cerebellum induces sprouting of uninjured purkinje cell axons. J. Neurosci. 2000, 20(6):2275-2286.
13. Burns S.P., et al. Recovery of ambulation in motor-incomplete tetraplegia. Arch. Phys. Med. Rehabil. 1997, 78(11):1169-1172.
14. Cafferty W.B., et al. Response to correspondence: Kim et al., "axon regeneration in young adult mice lacking Nogo-A/B." Neuron 38, 187-199. Neuron 2007, 54(2):195-199.
15. Cafferty W.B., et al. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J. Neurosci. 2007, 27(9):2176-2185.
16. Cafferty W.B.J., McGee A.W., Strittmatter S.M. Axonal growth therapeutics: regeneration or sprouting or plasticity?. Trends Neurosci. 2008, 31(5):215-220.
17. Cafferty W.B.J., et al. MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J. Neurosci. 2010, 30(20):6825-6837.
18. Cajal S.R.y. Cajal's Degeneration and Regeneration of the Nervous System 1991, 976. Oxford Univeristy Press.
19. 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. 1988, 106(4):1281-1288.
20. Chang K.-J., et al. Oligodendrocyte myelin glycoprotein does not influence node of ranvier structure or assembly. J. Neurosci. 2010, 30(43):14476-14481.
21. Chen M.S., et al. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000, 403(6768):434-439.
22. Chivatakarn O., et al. The Nogo-66 Receptor NgR1 is required only for the acute growth cone-collapsing but not the chronic growth-inhibitory actions of myelin inhibitors. J. Neurosci. 2007, 27(27):7117-7124.
23. Coumans J.V., et al. Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J. Neurosci. 2001, 21(23):9334-9344.
24. Crair M.C., Gillespie D.C., Stryker M.P. The role of visual experience in the development of columns in cat visual cortex. Science 1998, 279(5350):566-570.
25. David S., Aguayo A. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 1981, 214(4523):931-933.
26. Dimou L., et al. Nogo-A-deficient mice reveal strain-dependent differences in axonal regeneration. J. Neurosci. 2006, 26(21):5591-5603.
27. Fouad K., Klusman I., Schwab M.E. Regenerating corticospinal fibers in the Marmoset (Callitrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. Eur. J. Neurosci. 2004, 20(9):2479-2482.
28. Fournier A.E., GrandPre T., Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409(6818):341-346.
29. Fournier A.E., et al. Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. J. Neurosci. 2002, 22(20):8876-8883.
30. Fournier A.E., Takizawa B.T., Strittmatter S.M. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci. 2003, 23(4):1416-1423.
31. Freund P., et al. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat. Med. 2006, 12(7):790-792.
32. Freund P., et al. Anti-Nogo-A antibody treatment enhances sprouting of corticospinal axons rostral to a unilateral cervical spinal cord lesion in adult macaque monkey. J. Comp. Neurol. 2007, 502(4):644-659.
33. Freund P., et al. Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates - re-examination and extension of behavioral data. Eur. J. Neurosci. 2009, 29(5):983-996.
34. Geisler F.H.C., William P., Grieco Giacinto, Poonian Devinder Measurements and recovery patterns in a multicenter study of acute spinal cord injury. Spine 2001, 26(24S):S68-S86. the Sygen Study Group.
35. GrandPre T., et al. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 2000, 403(6768):439-444.
36. GrandPre T., Li S., Strittmatter S.M. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 2002, 417(6888):547-551.
37. Habib A.A., et al. Expression of the oligodendrocyte-myelin glycoprotein by neurons in the mouse central nervous system. J. Neurochem. 1998, 70(4):1704-1711.
38. Hensch T.K., Stryker M.P. Columnar architecture sculpted by GABA circuits in developing cat visual cortex. Science 2004, 303(5664):1678-1681.
39. Higley M.J., Strittmatter S.M. Neuroscience. Lynx for braking plasticity. Science 2010, 330(6008):1189-1190.
40. Hsieh S.H.-K., Ferraro G.B., Fournier A.E. Myelin-associated inhibitors regulate cofilin phosphorylation and neuronal inhibition through LIM kinase and Slingshot phosphatase. J. Neurosci. 2006, 26(3):1006-1015.
41. Hu F., Strittmatter S.M. The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. J. Neurosci. 2008, 28(5):1262-1269.
42. Huang Z.J., et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98(6):739-755.
43. Huang J.K., et al. Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 2005, 310(5755):1813-1817.
44. Huber A.B., et al. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J. Neurosci. 2002, 22(9):3553-3567.
45. Huebner E.A., et al. A multi-domain fragment of nogo-a is a potent inhibitor of cortical axon regeneration via nogo receptor 1. J. Biol. Chem. 2011, 286(20):18026-18036.
46. Ji B., et al. Assessment of functional recovery and axonal sprouting in oligodendrocyte-myelin glycoprotein (OMgp) null mice after spinal cord injury. Mol. Cell. Neurosci. 2008, 39(2):258-267.
47. Josephson A., et al. NOGO mRNA expression in adult and fetal human and rat nervous tissue and in weight drop injury. Exp. Neurol. 2001, 169(2):319-328.
48. Kakulas B. The clinical neuropathology of spinal cord injury. A guide to the future. Paraplegia 1987, 25(3):212-216.
49. Karlen A., et al. Nogo receptor 1 regulates formation of lasting memories. Proc. Natl Acad. Sci. 2009, 106(48):20476-20481.
50. Kim J.-E., et al. Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 2003, 38(2):187-199.
51. Kim J.E., et al. Nogo-C is sufficient to delay nerve regeneration. Mol. Cell. Neurosci. 2003, 23(3):451-459.
52. Kim J.E., et al. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 2004, 44(3):439-451.
53. Kottis V., et al. Oligodendrocyte-myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. J. Neurochem. 2002, 82(6):1566-1569.
54. Kubagawa H., Burrows P.D., Cooper M.D. A novel pair of immunoglobulin-like receptors expressed by B cells and myeloid cells. Proc. Natl Acad. Sci. U. S. A. 1997, 94(10):5261-5266.
55. Lai C., et al. 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, 84(12):4337-4341.
56. Lee J.K., et al. Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J. Neurosci. 2004, 24(27):6209-6217.
57. Lee H., et al. Synaptic function for the Nogo-66 receptor NgR1: regulation of dendritic spine morphology and activity-dependent synaptic strength. J. Neurosci. 2008, 28(11):2753-2765.
58. Lee J.K., et al. Assessing spinal axon regeneration and sprouting in Nogo- , MAG- , and OMgp-deficient mice. Neuron 2010, 66(5):663-670.
59. Li S., Strittmatter S.M. Delayed systemic Nogo-66 receptor antagonist promotes recovery from spinal cord injury. J. Neurosci. 2003, 23(10):4219-4227.
60. Li M., et al. Myelin-associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse. J. Neurosci. Res. 1996, 46(4):404-414.
61. Li S., et al. Blockade of nogo-66, myelin-associated glycoprotein, and oligodendrocyte myelin glycoprotein by soluble nogo-66 receptor promotes axonal sprouting and recovery after spinal injury. J. Neurosci. 2004, 24(46):10511-10520.
62. Li S., et al. Transgenic inhibition of Nogo-66 receptor function allows axonal sprouting and improved locomotion after spinal injury. Mol. Cell. Neurosci. 2005, 29(1):26-39.
63. Liebscher T., et al. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann. Neurol. 2005, 58(5):706-719.
64. Liebscher T., et al. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann. Neurol. 2005, 58(5):706-719.
65. Liu B.P., et al. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002, 297(5584):1190-1193.
66. McGee A.W., et al. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 2005, 309(5744):2222-2226.
67. McKerracher L., et al. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 1994, 13(4):805-811.
68. Mi S., et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 2004, 7(3):221-228.
69. Mikol D.D., Stefansson K. A phosphatidylinositol-linked peanut agglutinin-binding glycoprotein in central nervous system myelin and on oligodendrocytes. J. Cell Biol. 1988, 106(4):1273-1279.
70. Montani L., et al. Neuronal Nogo-A modulates growth cone motility via Rho-GTP/LIMK1/Cofilin in the unlesioned adult nervous system. J. Biol. Chem. 2009, 284(16):10793-10807.
71. Moon L.D., et al. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 2001, 4(5):465-466.
72. Morishita H., et al. Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 2010, 330(6008):1238-1240.
73. Mukhopadhyay G., et al. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 1994, 13(3):757-767.
74. -/- mice. Nat. Immunol. 2004, 5(6):623-629.
75. Nakamura Y., et al. Paired immunoglobulin-like receptor B knockout does not enhance axonal regeneration or locomotor recovery after spinal cord injury. J. Biol. Chem. 2011, 286(3):1876-1883.
76. Ng W.P., et al. Myelin from MAG-deficient mice is a strong inhibitor of neurite outgrowth. Neuroreport 1996, 7(4):861-864.
77. Niederost B., et al. Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J. Neurosci. 2002, 22(23):10368-10376.
78. Oertle T., et al. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J. Neurosci. 2003, 23(13):5393-5406.
79. Omoto S., et al. Genetic deletion of paired immunoglobulin-like receptor B Does not promote axonal plasticity or functional recovery after traumatic brain injury. J. Neurosci. 2010, 30(39):13045-13052.
80. Park J.B., et al. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005, 45(3):345-351.
81. Park J.H., et al. Subcutaneous Nogo Receptor removes brain Amyloid-{beta} and improves spatial memory in Alzheimer's transgenic mice. J. Neurosci. 2006, 26(51):13279-13286.
82. Pizzorusso T., et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298(5596):1248-1251.
83. Pot C., et al. Nogo-A expressed in Schwann cells impairs axonal regeneration after peripheral nerve injury. J. Cell Biol. 2002, 159(1):29-35.
84. Prinjha R., et al. Neurobiology: inhibitor of neurite outgrowth in humans. Nature 2000, 403(6768):383-384.
85. Raiker S.J., et al. Oligodendrocyte-myelin glycoprotein and nogo negatively regulate activity-dependent synaptic plasticity. J. Neurosci. 2010, 30(37):12432-12445.
86. Richard M., et al. Neuronal expression of Nogo-A mRNA and protein during neurite outgrowth in the developing rat olfactory system. Eur. J. Neurosci. 2005, 22(9):2145-2158.
87. Richardson P.M., McGuinness U.M., Aguayo A.J. Axons from CNS neurones regenerate into PNS grafts. Nature 1980, 284(5753):264-265.
88. Robak L.A., et al. Molecular basis of the interactions of the Nogo-66 receptor and its homolog NgR2 with myelin-associated glycoprotein: development of NgROMNI-Fc, a novel antagonist of CNS myelin inhibition. J. Neurosci. 2009, 29(18):5768-5783.
89. Saneyoshi T., Fortin D.A., Soderling T.R. Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr. Opin. Neurobiol. 2010, 20(1):108-115.
90. Savio T., Schwab M. Rat CNS white matter, but not gray matter, is nonpermissive for neuronal cell adhesion and fiber outgrowth. J. Neurosci. 1989, 9(4):1126-1133.
91. Schnell L., Schwab M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 1990, 343(6255):269-272.
92. Schwab M., Schnell L. Channeling of developing rat corticospinal tract axons by myelin-associated neurite growth inhibitors. J. Neurosci. 1991, 11(3):709-721.
93. Science A.I.f.B. Allen Spinal Cord Atlas [Internet] 2009.
94. Seymour A.B., et al. Delayed treatment with monoclonal antibody IN-1 1week after stroke results in recovery of function and corticorubral plasticity in adult rats. J. Cereb. Blood Flow Metab. 2005, 25(10):1366-1375.
95. Shao Z., et al. TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 2005, 45(3):353-359.
96. Simonen M., et al. Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 2003, 38(2):201-211.
97. Syken J., et al. PirB restricts ocular-dominance plasticity in visual cortex. Science 2006, 313(5794):1795-1800.
98. Takai T., Ono M. Activating and inhibitory nature of the murine paired immunoglobulin-like receptor family. Immunol. Rev. 2001, 181(1):215-222.
99. Thallmair M., et al. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci. 1998, 1(2):124-131.
100. Trapp B.D. Myelin-associated glycoprotein location and potential functionsa. Ann. N. Y. Acad. Sci. 1990, 605(1):29-43.
101. Vargas M.E., Barres B.A. Why is Wallerian degeneration in the CNS so slow?. Annu. Rev. Neurosci. 2007, 30(1):153-179.
102. Venkatesh K., et al. The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J. Neurosci. 2005, 25(4):808-822.
103. Wang X., et al. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 2002, 22(13):5505-5515.
104. Wang K.C., et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002, 417(6892):941-944.
105. Wang K.C., et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002, 417(6892):941-944.
106. Wang X., et al. Delayed Nogo receptor therapy improves recovery from spinal cord contusion. Ann. Neurol. 2006, 60(5):540-549.
107. Woolf C.J. No Nogo: now where to go?. Neuron 2003, 38(2):153-156.
108. Zagrebelsky M., et al. Nogo-A stabilizes the architecture of hippocampal neurons. J. Neurosci. 2010, 30(40):13220-13234.
109. Z'Graggen W.J., et al. Functional recovery and enhanced corticofugal plasticity after unilateral pyramidal tract lesion and blockade of myelin-associated neurite growth inhibitors in adult rats. J. Neurosci. 1998, 18(12):4744-4757.
110. Zheng B., et al. Lack of enhanced spinal regeneration in nogo-deficient mice. Neuron 2003, 38(2):213-224.