The injured and regenerating nervous system: Immunoglobulin superfamily members as key players

Neuroscientist

Volumn 18, Issue 5, 2012, Pages 452-466

  Irintchev, Andrey ^a   Schachner, Melitta ^b,c  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

close homologue of L1; injury; L1; myelin associated glycoprotein; nervous system; neural cell adhesion molecule; peripheral nerve; regeneration; spinal cord

Indexed keywords

GLYCAN; IMMUNOGLOBULIN; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE L1; POLYSIALIC ACID;

CELL REGENERATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MYELINATION; NERVE CELL PLASTICITY; NERVE FIBER MEMBRANE POTENTIAL; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INJURY; NEUROPROTECTION; NEUROSCIENCE; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL ADHESION MOLECULES; CENTRAL NERVOUS SYSTEM; HUMANS; MYELIN SHEATH; NERVE REGENERATION; NEURAL CELL ADHESION MOLECULE L1; NEURAL CELL ADHESION MOLECULES; NEURONAL PLASTICITY; NEURONS; NEUROPROTECTIVE AGENTS; PERIPHERAL NERVOUS SYSTEM;

EID: 84866707752     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858411419047     Document Type: Review

References (123)

1. Apostolova I, Irintchev A, Schachner M. Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice. J Neurosci. 2006 ; 26 (30). 7849-59
2. Atwal JK, Pinkston-Gosse J, Syken J, Stawicki S, Wu Y, Shatz C. PirB is a functional receptor formyelin inhibitors of axonal regeneration. Science. 2008 ; 322 (5903). 967-70
3. Aubert I, Ridet JL, Schachner M, Rougon G, Gage FH. Expression of L1 and PSA during sprouting and regeneration in the adult hippocampal formation. J Comp Neurol. 1998 ; 399 (1). 1-19
4. Ballermann M, Fouad K. Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers. Eur J Neurosci. 2006 ; 23 (8). 1988-96
5. Barclay AN. Membrane proteins with immunoglobulin-like domains-a master superfamily of interaction molecules. Semin Immunol. 2003 ; 15 (4). 215-23
6. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci. 2004 ; 7 (3). 269-77
7. Bartsch U, Bandtlow CE, Schnell L, Bartsch S, Spillmann AA, Rubin BP. Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron. 1995 ; 15 (6). 1375-81
8. 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). 451-62
9. Becker CG, Becker T. Growth and pathfinding of regenerating axons in the optic projection of adult fish. J Neurosci Res. 2007a ; 85 (12). 2793-9
10. Becker CG, Becker T Model organisms in spinal cord regeneration. Weinheim, Germany: John Wiley ; 2007b :
11. Becker CG, Becker T, Meyer RL. Increased NCAM-180 immunoreactivity and maintenance of L1 immunoreactivity in injured optic fibers of adult mice. Exp Neurol. 2001 ; 169 (2). 438-48
12. Becker T, Lieberoth BC, Becker CG, Schachner M. Differences in the regenerative response of neuronal cell populations and indications for plasticity in intraspinal neurons after spinal cord transection in adult zebrafish. Mol Cell Neurosci. 2005 ; 30 (2). 265-78
13. Becker CG, Lieberoth BC, Morellini F, Feldner J, Becker T, Schachner M. L1.1 is involved in spinal cord regeneration in adult zebrafish. J Neurosci. 2004 ; 24 (36). 7837-42
14. Bernreuther C, Dihné M, Johann V, Schiefer J, Cui Y, Hargus G. Neural cell adhesion molecule L1-transfected embryonic stem cells promote functional recovery after excitotoxic lesion of the mouse striatum. J Neurosci. 2006 ; 26 (45). 11532-9
15. Blackmore M, Letourneau PC. Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J Neurobiol. 2006a ; 66 (4). 348-60
16. Blackmore M, Letourneau PC. L1, beta1 integrin, and cadherins mediate axonal regeneration in the embryonic spinal cord. J Neurobiol. 2006b ; 66 (14). 1564-83
17. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol. 2006 ; 80 (3). 129-64
18. Brushart T. Preferential reinnervation of motor nerves by regenerating motor axons. J Neurosci. 1988 ; 8 (3). 1026-31
19. Brümmendorf T, Rathjen FG. Structure/function relationships of axon-associated adhesion receptors of the immunoglobulin superfamily. Curr Opin Neurobiol. 1996 ; 6 (5). 584-93
20. Camand E, Morel MP, Faissner A, Sotelo C, Dusart I. Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur J Neurosci. 2004 ; 20 (5). 1161-76
21. Campbell DG, Williams AF, Bayley PM, Reid KB. Structural similarities between Thy-1 antigen from rat brain and immunoglobulin. Nature. 1979 ; 282 (5736). 341-2
22. Carenini S, Montag D, Schachner M, Martini R. Subtle roles of neural cell adhesion molecule and myelin-associated glycoprotein during Schwann cell spiralling in P0-deficient mice. Glia. 1999 ; 27 (3). 203-12
23. Carmichael ST. Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol. 2006 ; 59 (5). 735-42
24. Chaisuksunt V, Campbell G, Zhang Y, Schachner M, Lieberman AR, Anderson PN. The cell recognition molecule CHL1 is strongly upregulated by injured and regenerating thalamic neurons. J Comp Neurol. 2000 ; 425 (3). 382-92
25. Chaisuksunt V, Zhang Y, Anderson PN, Campbell G, Vaudano E, Schachner M. Axonal regeneration from CNS neurons in the cerebellum and brainstem of adult rats: correlation with the patterns of expression and distribution of messenger RNAs for L1, CHL1, c-jun and growth-associated protein-43. Neuroscience. 2000 ; 100 (1). 87-108
26. Charles P, Hernandez MP, Stankoff B, Aigrot MS, Colin C, Rougon G. Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci USA. 2000 ; 97 (13). 7585-90
27. Charles P, Reynolds R, Seilhean D, Rougon G, Aigrot MS, Niezgoda A. Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis?. Brain. 2002 ; 125 (Pt 9). 1972-9
28. Chaudhry N, de Silva U, Smith GM. Cell adhesion molecule L1 modulates nerve-growth-factor-induced CGRP-IR fiber sprouting. Exp Neurol. 2006 ; 202 (1). 238-49
29. Chen J, Bernreuther C, Dihné M, Schachner M. Cell adhesion molecule L-transfected embryonic stem cells with enhanced survival support regrowth of corticospinal tract axons in mice after spinal cord injury. J Neurotrauma. 2005 ; 22 (8). 896-906
30. Chen J, Wu J, Apostolova I, Skup M, Irintchev A, Kügler S. Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury. Brain. 2007 ; 130 (Pt 4). 954-69
31. Chen S, Mantei N, Dong L, Schachner M. Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J Neurobiol. 1999 ; 38 (3). 428-39
32. Chipman PH, Franz CK, Nelson A, Schachner M, Rafuse VF. Neural cell adhesion molecule is required for stability of reinnervated neuromuscular junctions. Eur J Neurosci. 2010 ; 31 (2). 238-49
33. Courtine G, Song B, Roy RR, Zhong H, Herrmann JE, Ao Y. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med. 2008 ; 14 (1). 69-74
34. Cui YF, Hargus G, Xu JC, Schmid JS, Shen YQ, Glatzel M. Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery in Parkinsonian mice. Brain. 2010 ; 133 (Pt 1). 189-204
35. Cunningham BA. Cell adhesion molecules as morphoregulators. Curr Opin Cell Biol. 1995 ; 7 (5). 628-33
36. Dahme M, Bartsch U, Martini R, Anliker B, Schachner M, Mantei N. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet. 1997 ; 17 (3). 346-9
37. Descalzi G, Kim S, Zhuo M. Presynaptic and postsynaptic cortical mechanisms of chronic pain. Mol Neurobiol. 2009 ; 40 (3). 253-9
38. Deumens R, Lübbers M, Jaken RJ, Meijs MF, Thurlings RM, Honig WM. Mice lacking L1 have reduced CGRP fibre in-growth into spinal transection lesions. Neurosci Lett. 2007 ; 420 (3). 277-81
39. Di Filippo M, Tozzi A, Costa C, Belcastro V, Tantucci M, Picconi B. Plasticity and repair in the post-ischemic brain. Neuropharmacology. 2008 ; 55 (3). 353-62
40. Dityatev A, Bukalo O, Schachner M. Modulation of synaptic transmission and plasticity by cell adhesion and repulsion molecules. Neuron Glia Biol. 2008 ; 4 (3). 197-209
41. Doherty P, Williams G, Williams EJ. CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol Cell Neurosci. 2000 ; 16 (4). 283-95
42. Dusart I, Morel MP, Wehrlé R, Sotelo C. Late axonal sprouting of injured Purkinje cells and its temporal correlation with permissive changes in the glial scar. J Comp Neurol. 1999 ; 408 (3). 399-418
43. Duveau V, Arthaud S, Rougier A, Le Gal La Salle G. Polysialylation of NCAM is upregulated by hyperthermia and participates in heat shock preconditioning-induced neuroprotection. Neurobiol Dis. 2007 ; 26 (2). 385-95
44. Duveau V, Fritschy JM. PSA-NCAM-dependent GDNF signaling limits neurodegeneration and epileptogenesis in temporal lobe epilepsy. Eur J Neurosci. 2010 ; 32 (1). 89-98
45. El Maarouf A, Petridis AK, Rutishauser U. Use of polysialic acid in repair of the central nervous system. Proc Natl Acad Sci USA. 2006 ; 103 (45). 16989-94
46. Emery DL, Raghupathi R, Saatman KE, Fischer I, Grady MS, McIntosh TK. Bilateral growth-related protein expression suggests a transient increase in regenerative potential following brain trauma. J Comp Neurol. 2000 ; 424 (3). 521-31
47. Fawcett J. Molecular control of brain plasticity and repair. Prog Brain Res. 2009 ; 175: 501-9
48. Fey A, Schachner M, Irintchev A. A novel motion analysis approach reveals late recovery in C57BL/6 mice and deficits in NCAM-deficient mice after sciatic nerve crush. J Neurotrauma. 2010 ; 27 (5). 815-28
49. Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci. 2003 ; 4 (9). 703-13
50. Fitch MT, Silver J. CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol. 2008 ; 209 (2). 294-301
51. Fox GB, Kjøller C, Murphy KJ, Regan CM. The modulations of NCAM polysialylation state that follow transient global ischemia are brief on neurons but enduring on glia. J Neuropathol Exp Neurol. 2001 ; 60 (2). 132-40
52. Franz C, Rutishauser U, Rafuse V. Intrinsic neuronal properties control selective targeting of regenerating motoneurons. Brain. 2008 ; 131 (Pt 6). 1492-505
53. Franz CK, Rutishauser U, Rafuse VF. Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons. J Neurosci. 2005 ; 25 (8). 2081-91
54. Giger RJ, Hollis ER, Tuszynski MH. Guidance molecules in axon regeneration. Cold Spring Harb Perspect Biol. 2010 ; 2 (7). a001867
55. Guseva D, Angelov D, Irintchev A, Schachner M. Ablation of adhesion molecule L1 in mice favours Schwann cell proliferation and functional recovery after peripheral nerve injury. Brain. 2009 ; 132 (Pt 8). 2180-95
56. Guseva D, Zerwas M, Xiao MF, Jakovcevski I, Irintchev A, Schachner M. Adhesion molecule L1 overexpressed under the control of the neuronal Thy-1 promoter improves myelination after peripheral nerve injury in adult mice. Exp Neurol. 2011 ; 229 (2). 339-52
57. Gwak YS, Hulsebosch CE. GABA and central neuropathic pain following spinal cord injury. Neuropharmacology. 2011 ; 60 (5). 799-808
58. Hildebrand C, Kocsis JD, Berglund S, Waxman SG. Myelin sheath remodelling in regenerated rat sciatic nerve. Brain Res. 1985 ; 358 (1-2). 163-70
59. Hillenbrand R, Molthagen M, Montag D, Schachner M. The close homologue of the neural adhesion molecule L1 (CHL1): patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur J Neurosci. 1999 ; 11 (3). 813-26
60. Holm J, Hillenbrand R, Steuber V, Bartsch U, Moos M, Lübbert H. Structural features of a close homologue of L1 (CHL1) in the mouse: a new member of the L1 family of neural recognition molecules. Eur J Neurosci. 1996 ; 8 (8). 1613-29
61. Horinouchi K, Nakamura Y, Yamanaka H, Watabe T, Shiosaka S. Distribution of L1cam mRNA in the adult mouse brain: in situ hybridization and Northern blot analyses. J Comp Neurol. 2005 ; 482 (4). 386-404
62. Hortsch M. Neural cell adhesion molecules-brain glue and much more!. Front Biosci. 2003 ; 8: d357-9
63. Hoschouer EL, Yin FQ, Jakeman LB. L1 cell adhesion molecule is essential for the maintenance of hyperalgesia after spinal cord injury. Exp Neurol. 2009 ; 216 (1). 22-34
64. Irving EA, Vinson M, Rosin C, Roberts JC, Chapman DM, Facci L. Identification of neuroprotective properties of anti-MAG antibody: a novel approach for the treatment of stroke?. J Cereb Blood Flow Metab. 2005 ; 25 (1). 98-107
65. Jakovcevski I, Mo Z, Zecevic N. Down-regulation of the axonal polysialic acid-neural cell adhesion molecule expression coincides with the onset of myelination in the human fetal forebrain. Neuroscience. 2007 ; 149 (2). 328-37
66. Jakovcevski I, Wu J, Karl N, Leshchyns'ka I, Sytnyk V, Chen J. Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J Neurosci. 2007 ; 27 (27). 7222-33
67. Jucker M, D'Amato F, Mondadori C, Mohajeri H, Magyar J, Bartsch U. Expression of the neural adhesion molecule L1 in the deafferented dentate gyrus. Neuroscience. 1996 ; 75 (3). 703-15
68. Jucker M, Mondadori C, Mohajeri H, Bartsch U, Schachner M. Transient upregulation of NCAM mRNA in astrocytes in response to entorhinal cortex lesions and ischemia. Brain Res Mol Brain Res. 1995 ; 28 (1). 149-56
69. Jung M, Petrausch B, Stuermer CA. Axon-regenerating retinal ganglion cells in adult rats synthesize the cell adhesion molecule L1 but not TAG-1 or SC-1. Mol Cell Neurosci. 1997 ; 9 (2). 116-31
70. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Schut D, Fehlings MG. Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci. 2010 ; 30 (5). 1657-76
71. Kim BG, Dai HN, McAtee M, Vicini S, Bregman BS. Remodeling of synaptic structures in the motor cortex following spinal cord injury. Exp Neurol. 2006 ; 198 (2). 401-15
72. Kim JE, Liu BP, Park JH, Strittmatter SM. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron. 2004 ; 44 (3). 439-51
73. Kleene R, Schachner M. Glycans and neural cell interactions. Nat Rev Neurosci. 2004 ; 5 (3). 195-208
74. Klementiev B, Novikova T, Korshunova I, Berezin V, Bock E. The NCAM-derived P2 peptide facilitates recovery of cognitive and motor function and ameliorates neuropathology following traumatic brain injury. Eur J Neurosci. 2008 ; 27 (11). 2885-96
75. Kruse J, Mailhammer R, Wernecke H, Faissner A, Sommer I, Goridis C. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature. 1984 ; 311 (5982). 153-5
76. Langenfeld-Oster B, Faissner A, Irintchev A, Wernig A. Polyclonal antibodies against NCAM and tenascin delay endplate reinnervation. J Neurocytol. 1994 ; 23 (19). 591-604
77. Lavdas AA, Chen J, Papastefanaki F, Chen S, Schachner M, Matsas R. Schwann cells engineered to express the cell adhesion molecule L1 accelerate myelination and motor recovery after spinal cord injury. Exp Neurol. 2010 ; 221 (1). 206-16
78. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, Leal MA. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron. 2010 ; 66 (5). 663-70
79. Loers G, Chen S, Grumet M, Schachner M. Signal transduction pathways implicated in neural recognition molecule L1 triggered neuroprotection and neuritogenesis. J Neurochem. 2005 ; 92 (6). 1463-76
80. Loers G, Schachner M. Recognition molecules and neural repair. J Neurochem. 2007 ; 101 (4). 865-82
81. Lundborg G, Rosén B. Hand function after nerve repair. Acta Physiol (Oxf). 2007 ; 189 (2). 207-17
82. Maness PF, Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci. 2007 ; 10 (1). 19-26
83. Marino P, Norreel JC, Schachner M, Rougon G, Amoureux MC. A polysialic acid mimetic peptide promotes functional recovery in a mouse model of spinal cord injury. Exp Neurol. 2009 ; 219 (1). 163-74
84. Martini R. Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J Neurocytol. 1994 ; 23 (1). 1-28
85. Martini R, Schachner M. Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and myelin-associated glycoprotein) in regenerating adult mouse sciatic nerve. J Cell Biol. 1988 ; 106 (5). 1735-46
86. Martini R, Schachner M, Brushart TM. The L2/HNK-1 carbohydrate is preferentially expressed by previously motor axon-associated Schwann cells in reinnervated peripheral nerves. J Neurosci. 1994 ; 14 (11, Pt 2). 7180-91
87. Mason MR, Lieberman AR, Anderson PN. Corticospinal neurons up-regulate a range of growth-associated genes following intracortical, but not spinal, axotomy. Eur J Neurosci. 2003 ; 18 (4). 789-802
88. Mears S, Schachner M, Brushart TM. Antibodies to myelin-associated glycoprotein accelerate preferential motor reinnervation. J Peripher Nerv Syst. 2003 ; 8 (2). 91-9
89. Mehanna A, Jakovcevski I, Acar A, Xiao M, Loers G, Rougon G. Polysialic acid glycomimetic promotes functional recovery and plasticity after spinal cord injury in mice. Mol Ther. 2010 ; 18 (1). 34-43
90. Mehanna A, Mishra B, Kurschat N, Schulze C, Bian S, Loers G. Polysialic acid glycomimetics promote myelination and functional recovery after peripheral nerve injury in mice. Brain. 2009 ; 132 (Pt 6). 1449-62
91. Meijs MF, Timmers L, Pearse DD, Tresco PA, Bates ML, Joosten EA. Basic fibroblast growth factor promotes neuronal survival but not behavioral recovery in the transected and Schwann cell implanted rat thoracic spinal cord. J Neurotrauma. 2004 ; 21 (10). 1415-30
92. Mishra B, von der Ohe M, Schulze C, Bian S, Makhina T, Loers G. Functional role of the interaction between polysialic acid and extracellular histone H1. J Neurosci. 2010 ; 30 (37). 12400-13
93. Murphy JA, Hartwick AT, Rutishauser U, Clarke DB. Endogenous polysialylated neural cell adhesion molecule enhances the survival of retinal ganglion cells. Invest Ophthalmol Vis Sci. 2009 ; 50 (2). 861-9
94. Nakamura Y, Fujita Y, Ueno M, Takai T, Yamashita T. Paired immunoglobulin-like receptor B knockout does not enhance axonal regeneration or locomotor recovery after spinal cord injury. J Biol Chem. 2011 ; 286 (3). 1876-83
95. Nikonenko A, Sun M, Lepsveridze E, Apostolova I, Petrova I, Irintchev A. Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1-deficient mice. Eur J Neurosci. 2006 ; 23 (7). 1839-52
96. Omoto S, Ueno M, Mochio S, Takai T, Yamashita T. 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). 13045-52
97. Ourednik V, Ourednik J, Xu Y, Zhang Y, Lynch WP, Snyder EY. Cross-talk between stem cells and the dysfunctional brain is facilitated by manipulating the niche: evidence from an adhesion molecule. Stem Cells. 2009 ; 27 (11). 2846-56
98. Papastefanaki F, Chen J, Lavdas AA, Thomaidou D, Schachner M, Matsas R. Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain. 2007 ; 130 (Pt 8). 2159-74
99. Quarles RH. Myelin-associated glycoprotein (MAG): past, present and beyond. J Neurochem. 2007 ; 100 (6). 1431-48
100. Roonprapunt C, Huang W, Grill R, Friedlander D, Grumet M, Chen S. Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury. J Neurotrauma. 2003 ; 20 (9). 871-82
101. Rougon G, Hobert O. New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci. 2003 ; 26: 207-38
102. Runyan SA, Roy RR, Zhong H, Phelps PE. L1 cell adhesion molecule is not required for small-diameter primary afferent sprouting after deafferentation. Neuroscience. 2007 ; 150 (4). 959-69
103. Sakai A, Asada M, Seno N, Suzuki H. Involvement of neural cell adhesion molecule signaling in glial cell line-derived neurotrophic factor-induced analgesia in a rat model of neuropathic pain. Pain. 2008 ; 137 (2). 378-88
104. Schäfer M, Fruttiger M, Montag D, Schachner M, Martini R. Disruption of the gene for the myelin-associated glycoprotein improves axonal regrowth along myelin in C57BL/Wlds mice. Neuron. 1996 ; 16 (6). 1107-13
105. Schmid RS, Maness PF. L1 and NCAM adhesion molecules as signaling coreceptors in neuronal migration and process outgrowth. Curr Opin Neurobiol. 2008 ; 18 (3). 245-50
106. Scholz T, Krichevsky A, Sumarto A, Jaffurs D, Wirth GA, Paydar K. Peripheral nerve injuries: an international survey of current treatments and future perspectives. J Reconstr Microsurg. 2009 ; 25 (6). 339-44
107. Shapiro L, Love J, Colman DR. Adhesion molecules in the nervous system: structural insights into function and diversity. Annu Rev Neurosci. 2007 ; 30: 451-74
108. Simova O, Irintchev A, Mehanna A, Liu J, Dihne M, Bachle D. Carbohydrate mimics promote functional recovery after peripheral nerve repair. Ann Neurol. 2006 ; 60 (4). 430-7
109. Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010 ; 119 (1). 7-35
110. Styren SD, Miller PD, Lagenaur CF, DeKosky ST. Alternate strategies in lesion-induced reactive synaptogenesis: differential expression of L1 in two populations of sprouting axons. Exp Neurol. 1995 ; 131 (2). 165-73
111. Teng YD, Mocchetti I, Taveira-DaSilva AM, Gillis RA, Wrathall JR. Basic fibroblast growth factor increases long-term survival of spinal motor neurons and improves respiratory function after experimental spinal cord injury. J Neurosci. 1999 ; 19 (16). 7037-47
112. Tomita K, Kubo T, Matsuda K, Yano K, Tohyama M, Hosokawa K. Myelin-associated glycoprotein reduces axonal branching and enhances functional recovery after sciatic nerve transection in rats. Glia. 2007 ; 55 (14). 1498-507
113. Troncoso E, Muller D, Korodi K, Steimer T, Welker E, Kiss JZ. Recovery of evoked potentials, metabolic activity and behavior in a mouse model of somatosensory cortex lesion: role of the neural cell adhesion molecule (NCAM). Cereb Cortex. 2004 ; 14 (3). 332-41
114. Walsh FS, Doherty P. Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. Annu Rev Cell Dev Biol. 1997 ; 13: 425-56
115. Woolf CJ, Mannion RJ. Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet. 1999 ; 353 (9168). 1959-64
116. Woolhead CL, Zhang Y, Lieberman AR, Schachner M, Emson PC, Anderson PN. Differential effects of autologous peripheral nerve grafts to the corpus striatum of adult rats on the regeneration of axons of striatal and nigral neurons and on the expression of GAP-43 and the cell adhesion molecules N-CAM and L1. J Comp Neurol. 1998 ; 391 (2). 259-73
117. Wu B, Ren X. Promoting axonal myelination for improving neurological recovery in spinal cord injury. J Neurotrauma. 2009 ; 26 (10). 1847-56
118. Yamanaka H, Obata K, Kobayashi K, Dai Y, Fukuoka T, Noguchi K. Alteration of the cell adhesion molecule L1 expression in a specific subset of primary afferent neurons contributes to neuropathic pain. Eur J Neurosci. 2007 ; 25 (4). 1097-111
119. Zhang S, Xia YY, Lim HC, Tang FR, Feng ZW. NCAM-mediated locomotor recovery from spinal cord contusion injury involves neuroprotection, axon regeneration, and synaptogenesis. Neurochem Int. 2010 ; 56 (8). 919-29
120. Zhang Y, Bo X, Schoepfer R, Holtmaat AJ, Verhaagen J, Emson PC. Growth-associated protein GAP-43 and L1 act synergistically to promote regenerative growth of Purkinje cell axons in vivo. Proc Natl Acad Sci USA. 2005 ; 102 (41). 14883-8
121. Zhang Y, Campbell G, Anderson PN, Martini R, Schachner M, Lieberman AR. Molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts: I. Neural cell adhesion molecules. J Comp Neurol. 1995 ; 361 (2). 193-209
122. Zhang Y, Roslan R, Lang D, Schachner M, Lieberman AR, Anderson PN. Expression of CHL1 and L1 by neurons and glia following sciatic nerve and dorsal root injury. Mol Cell Neurosci. 2000 ; 16 (1). 71-86
123. Zhang Y, Yeh J, Richardson PM, Bo X. Cell adhesion molecules of the immunoglobulin superfamily in axonal regeneration and neural repair. Restor Neurol Neurosci. 2008 ; 26 (2-3). 81-96