LINGO-1 antagonists as therapy for multiple sclerosis: In vitro and in vivo evidence

Expert Opinion on Biological Therapy

Volumn 8, Issue 10, 2008, Pages 1561-1570

  Rudick, Richard A ^a   Mi, Sha ^b   Sandrock Jr , Alfred W ^b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b BIOGEN   (United States)

Author keywords

Antagonists; LINGO 1; Multiple sclerosis; Preclinical

Indexed keywords

ENZYME INHIBITOR; IMMUNOGLOBULIN G; LENTIVIRUS VECTOR; LEUCINE RICH REPEATS AND IMMUNOGLOBULIN DOMAIN CONTAINING NEURITE OUTGROWTH INHIBITOR RECEPTOR INTERACTING PROTEIN; LEUCINE RICH REPEATS AND IMMUNOGLOBULIN DOMAIN CONTAINING NEURITE OUTGROWTH INHIBITOR RECEPTOR INTERACTING PROTEIN ANTAGONIST; LEUCINE RICH REPEATS AND IMMUNOGLOBULIN DOMAIN CONTAINING NEURITE OUTGROWTH INHIBITOR RECEPTOR INTERACTING PROTEIN FC FRAGMENT; MONOCLONAL ANTIBODY; MYELIN; NATURAL KILLER CELL RECEPTOR; NEURITE PROMOTING FACTOR; NEUROTROPHIN RECEPTOR P75; NOGO 66 RECEPTOR; NOGO A ANTIBODY; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PLATELET DERIVED GROWTH FACTOR A; PROTEIN KINASE FYN; PROTEIN NOGO; PROTEIN NOGO A; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ORPHAN Y; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; APOPTOSIS; CELL SURVIVAL; DEMYELINATION; DRUG TARGETING; HUMAN; MULTIPLE SCLEROSIS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PARKINSON DISEASE; REMYELINIZATION; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; VIRAL GENE DELIVERY SYSTEM;

CELL DIFFERENTIATION; HUMANS; MEMBRANE PROTEINS; MULTIPLE SCLEROSIS; NERVE TISSUE PROTEINS; OLIGODENDROGLIA;

EID: 54349085579     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.8.10.1561     Document Type: Review

References (70)

1. Sospedra M, Martin R. Immunology of multiple sclerosis. Ann Rev Immunol 2005;23:683-747
2. Dhib-Jalbut S. Pathogenesis of myelin/oligodendrocyte damage in multiple sclerosis. Neurology 2007;68(Suppl 3):S13-21
3. Dhib-Jalbut S, Arnold DL, Cleveland DW, et al. Neurodegeneration and neuroprotection in multiple sclerosis and other neurodegenerative diseases. J Neuroimmunol 2006;176:198-215
4. The International Multiple Sclerosis Genetics Consortium. Risk alleles for multiple sclerosis identified by a genomewide study. N Engl J Med 2007;357:851-62
5. Gregory SG, Schmidt S, Seth P, et al. Interleukin 7 receptor α chain (IL7R) shows allelic and functional association with multiple sclerosis. Nat Genet 2007;39:1083-91
6. Lundmark F, Duvefelt K, Iacobaeus E, et al. Variation in interleukin 7 receptor α chain (ILR) influences risk of multiple sclerosis. Nat Genet 2007;39:1108-13
7. Jack C, Ruffini F, Bar-Or A, Antel JR Microglia and multiple sclerosis. J Neurosci Res 2005;81:363-373
8. Antel J. Oligodendrocyte/myelin injury and repair as a function of the central nervous system environment. Clin Neurol Neurosurg 2006;108:245-9
9. Trapp BD, Peterson J, Ransohoff RM, et al. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998;338:278-85
10. Filippi M, Bozzali M, Rovaris M, et al. Evidence for widespread axonal damage at the earliest stage of multiple sclerosis. Brain 2003;126:433-7
11. Matthews PM, De Stefano N, Narayanan S, et al. Putting magnetic resonance spectroscopy studies in context: axonal damage and disability in multiple sclerosis. Semin Neurol 1998;18:327-36
12. Trapp BD, Ransohoff R, Fisher E, Rudick R. Neurodegeneration in multiple sclerosis: relationship to neurologic disability. Neuroscientist 1999;5:48-57
13. Ferguson B, Matyszak MK, Esiri MM, Perry VH. Axonal damage in acute multiple sclerosis lesions. Brain 1997;120:393-9
14. Bjartmar C, Trapp BD. Axonal and neuronal degeneration in multiple sclerosis: mechanisms and functional consequences. Curr Opin Neurol 2001;14:271-8
15. Barnett MH, Prineas JW. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 2004;55:458-68
16. Peterson JW, Bö L, Mörk S, et al. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001;50:389-400
17. Brück W. Inflammatory demyelination is not central to the pathogenesis of multiple sclerosis. J Neurol 2005:252(Suppl 5):V/10-5
18. Dutta R, Trapp BD. Pathogenesis of axonal and neuronal damage in multiple sclerosis. Neurology 2007;68(Suppl 3):S22-31
19. The IFNB Multiple Sclerosis Study Group. Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial. Neurology 1993;43:655-61
20. Johnson KP, Brooks BR, Cohen JA, et al.; Copolymer 1 Multiple Sclerosis Study Group. Copolymer 1 reduces relapse rate and improves disability in relapsing-remitting multiple sclerosis: results of a phase III multicenter, double-blind placebo-controlled trial. Neurology 1995;45:1268-76
21. Jacobs LD, Cookfair DL, Rudick RA, et al. Intramuscular interferon beta-1a for disease progression in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Ann Neurol 1996;39:285-94
22. PRISMS (Prevention of Relapses and Disability by Interferon β-1a Subcutaneously in Multiple Sclerosis) Study Group. Randomised double-blind placebo-controlled study of interferon β-1a in relapsing/ remitting multiple sclerosis. Lancer 1998;352:1498-504
23. Polman CH, O'Connor PW, Havrdova E, et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 2006;354:899-910
24. Zhao C, Fancy SPJ, Kotter MR, et al. Mechanisms of CNS remyelination - the key to therapeutic advances. J Neurol Sci 2005;233:87-91
25. Mi S, Sandrock A, Miller RH. LINGO-1 and its role in CNS repair. Int J Biochem Cell Biol 2008;40:1971-8
26. Chang A, Tourtellotte WW, Rudick R, Trapp BD. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002;346:165-73
27. Kuhlmann T, Miron V, Cuo Q, et al. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 2008;131:1749-58
28. Mi S, Miller RH, Lee X, et al. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 2005;8:745-51
29. Lee X, Yang Z, Shao Z, et al. NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J Neurosci 2007;27:220-5
30. Mi S, Lee X, Shao Z, et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 2004;7:221-8
31. Mosyak L, Wood A, Dwyer B, et al. The structure of the Lingo-1 ectodomain, a module implicated in central nervous system repair inhibition. J Biol Chem 2006;281:36378-90
32. Fournier AE, GrandPre T, Strittmatter SM. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001;409:341-6
33. Yamashita T, Higuchi H, Tohyama M. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J Cell Sci 2002;157:565-70
34. Wang KC, Kim JA, Sivasankaran R, et al. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002;420:74-8
35. Park JB, Yiu G, Kaneko S, et al. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005;45:345-51
36. Shao Z, Browning JL, Lee X, et al. TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 2005;45:353-9
37. Barrette B, Vallières N, Dubé M, Lacroix S. Expression profile of receptors for myelin-associated inhibitors of axonal regeneration in the intact and injured mouse central nervous system. Mol Cell Neurosci 2007;34:519-38
38. Chao MV. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 2003;4:299-309
39. GrandPré T, Nakamura F, Vartarian T, Strittmatter SM. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 2000;403:439-44
40. Oertle T, Van Der Haar ME, Bandtlow CE, et al. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J Neurosci 2003;23:5393-406
41. Domeniconi M, Cao Z, Spencer T, et al. Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 2002;35:283-90
42. Liu BP, Fournier A, GrandPré T, Strittmatter SM. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002;297:1190-3
43. Wang KC, Koprivica V, Kim JA, et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002;417:941-4
44. Huber AB, Weinmann O, Brösamle C, et al. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 2002;22:3553-67
45. Hasegawa Y, Fujitani M, Hata K, et al. Promotion of axon regeneration by myelin-associated glycoprotein and Nogo through divergent signals downstream of Gi/G. J Neurosci 2004;24:6826-32
46. Sivasankaran R, Pei J, Wang KC, et al. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci 2004;7:261-8
47. Yamashita T, Tohyama M. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 2003;6:461-7
48. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998;279:509-14
49. Zhao X-H, Jin W-L, Ju G. An in vitro study on the involvement of LINGO-1 and Rho GTPases in Nogo-A regulated differentiation of oligodendrocyte precursor cells. Mol Cell Neurosci 2007;36:260-9
50. Walmsley AR, Mir AK. Targeting the Nogo-A signaling pathway to promote recovery following acute CNS injury. Curr Pharm Des 2007; 13:2470-84
51. Fournier AE, Takizawa BT, Strittmatter SM. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 2003;23:1416-23
52. Miller RH, Mi S. Dissecting demyelination. Nat Neurosci 2007;10:1351-4
53. Calver AR, Hall AC, Yu WP, et al. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 1998;20:869-82
54. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJM. Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 2004;25:252-62
55. Zhou Q, Choi G, Anderson DJ. The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 2001;31:791-807
56. Wang S, Sdrulla AD, DiSibio G, et al. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 1998;21:63-75
57. Charles P, Hernandez MP, Stankoff B, et al. Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci USA 2000;97:7585-90
58. Arnett HA, Fancy SPJ, Alberta JA, et al. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 2004;306:2111-5
59. Fancy SPJ, Zhao C, Franklin RJM. Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol Cell Neurosci 2004;27:247-54
60. Chary DM. Remyelination in multiple sclerosis. Int Rev Neurobiol 2007;79:589-620
61. Raine CS, Wu E. Multiple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 1993;52:199-204
62. Patrikios P, Stadelmann C, Kutzelnigg A, et al. Remyetination is extensive in a subset of multiple sclerosis patients. Brain 2006;129:3165-72
63. Kotter MR, Li W-W, Zhao C, Franklin RJM. Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J Neurosci 2006;26:328-32
64. Karnezis T, Mandemakers W, McQualter JL, et al. The neurite outgrowth inhibitor Nogo A is involved in autoimmune-mediated demyelination. Nat Neurosci 2004;7:736-44
65. Mi S, Hu B, Hahm K, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med 2007;13:1228-33
66. Liang X, Draghi NA, Resh MD. Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 2004;24:7140-9
67. Liu XZ, Xu XM, Hu R, et al. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 1997;17:5395-406
68. Casha S, Yu WR, Fehlings MG. Oligodendroglial apoptosis occurs along degenerating axons and is associated with Fas and p75 expression following spinal cord injury in the rats. Neuroscience 2001;103:203-18
69. Ji B, Li M, Wu W-T, et al. LINGO-1 antagonist promotes functional recovery and axonal sprouting after spinal cord injury. Mol Cell Neurosci 2006;33:311-20
70. Inoue H, Lin L, Lee X, et al. Inhibition of the leucine-rich repeat protein LINGO-1 enhances survival, structure, and function of dopaminergic neurons in Parkinson's disease models. Proc Natl Acad Sci USA 2007;104:14430-5