Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury

Brain

Volumn 130, Issue 4, 2007, Pages 954-969

  Chen, Jian ^a   Wu, Junfang ^a   Apostolova, Ivayla ^b   Skup, Malgorzata ^c   Irintchev, Andrey ^b   Kügler, Sebastian ^d   Schachner, Melitta ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Adeno associated virus; Axonal regeneration; L1; Locomotor recovery; Spinal cord injury

Indexed keywords

FIBRONECTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE CELL ADHESION MOLECULE L1; PARVOVIRUS VECTOR; PROTEIN NG2; PROTEOCHONDROITIN SULFATE; SEROTONIN; UNCLASSIFIED DRUG; SEROTONIN RECEPTOR AFFECTING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GLIA; LOCOMOTION; LUMBAR SPINAL CORD; MOUSE; MUSCLE FUNCTION; NERVE CELL; NERVE FIBER; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL TRACT; REGENERATION; REINNERVATION; SPINAL CORD; SPINAL CORD COMPRESSION; SPINAL CORD INJURY; WALKING; ADENOVIRUS; ANIMAL; C57BL MOUSE; CELL DIVISION; CELL MOTION; CHEMISTRY; CONVALESCENCE; GENE EXPRESSION; GENE VECTOR; GENETICS; IMMUNOLOGY; MOVEMENT (PHYSIOLOGY); NERVE REGENERATION; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADENOVIRIDAE; ANIMALS; ASTROCYTES; AXONS; CELL DIVISION; CELL MOVEMENT; FEMALE; GENE EXPRESSION; GENETIC VECTORS; MICE; MICE, INBRED C57BL; MOVEMENT; NERVE REGENERATION; NEURAL CELL ADHESION MOLECULE L1; NEUROGLIA; NEURONS; RECOVERY OF FUNCTION; SEROTONIN; SEROTONIN AGENTS; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD INJURIES;

EID: 34249710683     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm049     Document Type: Article

References (92)

1. Adcock KH, Brown DJ, Shearer MC, Shewan D, Schachner M, Smith GM, et al. Axon behaviour at Schwann cell-astrocyte boundaries: manipulation of axon signalling pathways and the neural adhesion molecule L1 can enable axons to cross. Eur J Neurosci 2004; 20: 1425-35.
2. 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: 7849-59.
3. Appel F, Holm J, Conscience JF, Schachner M. Several extracellular domains of the neural cell adhesion molecule L1 are involved in neurite outgrowth and cell body adhesion. J Neurosci 1993; 13: 4764-75.
4. Appel F, Holm J, Conscience JF, von Bohlen und Halbach F, Faissner A, James P, et al. Identification of the border between fibronectin type III homologous repeats 2 and 3 of the neural cell adhesion molecule L1 as a neurite outgrowth promoting and signal transducing domain. J Neurobiol 1995; 28: 297-312.
5. Barbin G, Aigrot MS, Charles P, Foucher A, Grumet M, Schachner M, et al. Axonal cell-adhesion molecule L1 in CNS myelination. Neuron Glia Biol 2004; 2: 65-72.
6. Barbeau H, Rossignol S. Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. Brain Res 1991; 546: 250-60.
7. 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: 7837-42.
8. Beggs HE, Baragona SC, Hemperly JJ, Maness PF. NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J Biol Chem 1997; 272: 8310-9.
9. Berry M, Hubbard P, Butt AM. Cytology and lineage of NG2-positive glia. J Neurocytol 2002; 31: 457-67.
10. Bett AJ, Haddara W, Prevec L, Graham FL. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early refion 1 and 3. Proc Natl Acad Sci USA 1994; 91: 8802-6.
11. Buchli AD, Schwab ME. Inhibition of Nogo: a key strategy to increase regeneration, plasticity and functional recovery of the lesioned central nervous system. Ann Med 2005; 37: 556-67.
12. Capello E, Voskuhl RR, McFarland HF, Raine CS. Multiple sclerosis: re-expression of a developmental gene in chronic lesions correlates with remyelination. Ann Neurol 1997; 41: 797-805.
13. Castellani V, De Angelis E, Kenwrick S, Rougon G. Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J 2002; 21: 6348-57.
14. Causeret F, Hidalgo-Sanchez M, Fort P, Backer S, Popoff MR, Gauthier-Rouviere C, et al. Distinct roles of Rac1/Cdc42 and Rho/Rock for axon outgrowth and nucleokinesis of precerebellar neurons toward netrin 1. Development 2004; 131: 2841-52.
15. Chen J, Leong SY, Schachner M. Differential expression of cell fate determinants in neurons and glial cells of adult mouse spinal cord after compression injury. Eur J Neurosci 2005a; 22: 1895-906.
16. Chen J, Bernreuther C, Dihne M, Schachner M. Cell adhesion molecule L1-transfected embryonic stem cells with enhanced survival support regrowth of corticospinal tract axons in mice after spinal cord injury. J Neurotrauma 2005b; 22: 896-906.
17. Chierzi S, Ratto GM, Verma P, Fawcett JW. The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. Eur J Neurosci 2005; 21: 2051-62.
18. Crown ED, Grau JW. Evidence that descending serotonergic systems protect spinal cord plasticity against the disruptive effect of uncontrollable stimulation. Exp Neurol 2005; 196: 164-76.
19. Curtis R, Green D, Lindsay RM, Wilkin GP. Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J Neurocytol 1993; 22: 51-64.
20. Dong L, Chen S, Schachner M. Single chain Fv antibodies against neural cell adhesion molecule L1 trigger L1 functions in cultured neurons. Mol Cell Neurosci 2003; 22: 234-47.
21. Dong L, Chen S, Richter M, Schachner M. Single-chain variable fragment antibodies against the neural adhesion molecule CHL1 (close homolog of L1) enhance neurite outgrowth. J Neurosci Res 2002; 69: 437-47.
22. Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR. Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci 2004; 27: 145-67.
23. Engesser-Cesar C, Anderson AJ, Basso DM, Edgerton VR, Cotman CW. Voluntary wheel running improves recovery from a moderate spinal cord injury. J Neurotrauma 2005; 22: 157-71.
24. Fidler PS, Schuette K, Asher RA, Dobbertin A, Thornton SR, Calle-Patino Y, et al. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: the major axon-inhibitory proteoglycan is NG2. J Neurosci 1999; 19: 8778-88.
25. Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 2003; 4: 703-13.
26. Fitch MT, Silver J. Glial cell extracellular matrix: boundaries for axon growth in development and regeneration. Cell Tissue Res 1997; 290: 379-84.
27. Flotte TR. Gene therapy progress and prospects: recombinant adeno-associated virus (rAAV) vectors. Gene Ther 2004; 11: 805-10.
28. Fouad K, Pearson K. Restoring walking after spinal cord injury. Prog Neurobiol 2004; 73: 107-26.
29. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, Pearse DD. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J Neurosci 2005; 25: 1169-78.
30. Fransen E, D'Hooge R, Van Camp G, Verhoye M, Sijbers J, Reyniers E, et al. L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum Mol Genet 1998; 7: 999-1009.
31. Gao Y, Nikulina E, Mellado W, Filbin MT. Neurotrophins elevate cAMP to reach a threshold required to overcome inhibition by MAG through extracellular signal-regulated kinase-dependent inhibition of phosphodiesterase. J Neurosci 2003; 23: 11770-7.
32. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, et al. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 2004; 44: 609-21.
33. Goldshmit Y, Galea MP, Wise G, Bartlett PF, Turnley AM. Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J Neurosci 2004; 24: 10064-73.
34. Grimm D, Kay MA, Kleinschmitt JA. Helper virus-free, optically controllable, and two-plasmid-based production of adeno-associated virus vectors of serotypes 1-6. Mol Ther 2003; 7: 839-50.
35. Haney CA, Sahenk Z, Li C, Lemmon VP, Roder J, Trapp BD. Heterophilic binding of L1 on unmyelinated sensory axons mediates Schwann cell adhesion and is required for axonal survival. J Cell Biol 1999; 146: 1173-84.
36. Houle JD, Jin Y. Chronically injured supraspinal neurons exhibit only modest axonal dieback in response to a cervical hemisection lesion. Exp Neurol 2001; 169: 208-17.
37. Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 2002; 22: 2792-803.
38. Kamiguchi H, Yoshihara F. The role of endocytic L1 trafficking in polarized adhesion and migration of nerve growth cones. J Neurosci 2001; 21: 9194-203.
39. Kerschensteiner M, Schwab ME, Lichtman JW, Misgeld T. In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat Med 2005; 11: 572-7.
40. Kleene R, Yang H, Kutsche M, Schachner M. The neural recognition molecule L1 is a sialic acid-binding lectin for CD24, which induces promotion and inhibition of neurite outgrowth. J Biol Chem 2001; 276: 21656-63.
41. Kügler S, Lingor P, Schöll U, Zolothukin S, Bähr M. Differential transgene expression in brain cells in vivo and in vitro from AAV-2 vectors with small transcriptional control units. Virology 2003; 311: 89-95.
42. Law JW, Lee AY, Sun M, Nikonenko AG, Chung SK, Dityatev A, et al. Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J Neurosci 2003; 23: 10419-32.
43. Lee JK, Emch GS, Johnson CS, Wrathall JR. Effect of spinal cord injury severity on alterations of the H-reflex. Exp Neurol 2005; 196: 430-40.
44. Lehmann M, Fournier A, Selles-Navarro I, Dergham P, Sebok A, Leclerc N, et al. Inactivation of Rho signalling pathway promotes CNS axon regeneration. J Neurosci 1999; 19: 7537-47.
45. Lemmon V, Farr KL, Lagenaur C. L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 1989; 2: 1597-603.
46. Lindner J, Rathjen FG, Schachner M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 1983; 305: 427-30.
47. Loers G, Schachner M. Recognition molecules and neural repair. J Neurochem 2007. In press.
48. 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: 1463-76.
49. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 2004; 24: 6402-9.
50. Luthi A, Laurent JP, Figurov A, Muller D, Schachner M. Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 1994; 372: 777-9.
51. Malik JMI, Shevtsova Z, Bähr M, Kügler S. Long-term in vivo inhibition of CNS neurodegeneration by Bcl-Xl gene transfer. Mol Ther 2005; 11: 373-81.
52. Mandel RJ, Bruger C. Clinical trials in neurological disorders using AAV vectors: promises and challenges. Curr Opin Mol Ther 2004; 6: 482-90.
53. Mandel RJ, Manfredsson FP, Foust KD, Rising A, Reimsnider S, Nash K, et al. Recombinant adeno-associated viral vectors as therapeutic agents to treat neurological disorders. Mol Ther 2006; 13: 463-83.
54. McGee AW, Strittmatter SM. The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci 2003; 26: 193-8.
55. Menet V, Gimenez YRM, Sandillon F, Privat A. GFAP null astrocytes are a favorable substrate for neuronal survival and neurite growth. Glia 2000; 31: 267-72.
56. Menet V, Gimenez y Ribotta M, Chauvet N, Drian MJ, Lannoy J, et al. Inactivation of the glial fibrillary acidic protein gene, but not that of vimentin, improves neuronal survival and neurite growth by modifying adhesion molecule expression. J Neurosci 2001; 21: 6147-58.
57. Monnier PP, Sierra A, Schwab JM, Henke-Fahle S, Mueller BK. The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol Cell Neurosci 2003; 22: 319-30.
58. Moos M, Tacke R, Scherer H, Teplow D, Fruh K, Schachner M. Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature 1988; 334: 701-3.
59. Mueller BK, Mack H, Teusch N. Rho kinase, a promising drug target for neurological disorders. Nat Rev Drug Discov 2005; 4: 387-98.
60. Nishimura T, Fukata Y, Kato K, Yamaguchi T, Matsuura Y, Kamiguchi H, et al. CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat Cell Biol 2003; 5: 819-26.
61. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, et al. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 2004; 10: 610-6.
62. Pedraza L, Fidler L, Staugaitis SM, Colman DR. The active transport of myelin basic protein into the nucleus suggests a regulatory role in myelination. Neuron 1997; 18: 579-89.
63. Pekny M, Pekna M. Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol 2004; 204: 428-37.
64. Pekny M, Johansson CB, Eliasson C, Stakeberg J, Wallen A, Perlmann T, et al. Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J Cell Biol 1999; 145: 503-14.
65. Pennypacker KR, Hong JS, Mullis SB, Hudson PM, McMillian MK. Transcription factors in primary glial cultures: changes with neuronal interactions. Brain Res Mol Brain Res 1996; 37: 224-30.
66. Pradel G, Schmidt R, Schachner M. Involvement of L1.1 in memory consolidation after active avoidance conditioning in zebrafish. J Neurobiol 2000; 43: 389-403.
67. Pringle NP, Yu WP, Howell M, Colvin JS, Ornitz DM, Richardson WD. Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 2003; 130: 93-102.
68. Rathjen FG, Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J 1984; 3: 1-10.
69. Ribotta MG, Provencher J, Feraboli-Lohnherr D, Rossignol S, Privat A, Orsal D. Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level. J Neurosci 2000; 20: 5144-52.
70. Roonprapunt C, Huang W, Grill R, Friedlander D, Grumet M, Chen S, et al. Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury. J Neurotrauma 2003; 20: 871-82.
71. Runyan SA, Roy R, Zhong H, Phelps PE. L1 CAM expression in the superficial dorsal horn is derived from the dorsal root ganglion. J Comp Neurol 2005; 485: 267-79.
72. Schmid RS, Pruitt WM, Maness PF. A MAP kinase-signalling pathway mediates neurite outgrowth on L1 and requires Src-dependent endocytosis. J Neurosci 2000; 20: 4177-88.
73. Seilheimer B, Persohn E, Schachner M. Neural cell adhesion molecule expression is regulated by Schwann cell-neuron interactions in culture. J Cell Biol 1989; 108: 1909-15.
74. Shapiro S. Neurotransmission by neurons that use serotonin, noradrenaline, glutamate, glycine, and gamma-aminobutyric acid in the normal and injured spinal cord. Neurosurgery 1997; 40: 168-77.
75. Shevtsova Z, Malik JM, Michel U, Bahr M, Kugler S. Promoters and serotypes: targeting of adeno-associated virus vectors for gene transfer in the rat central nervous system in vitro and in vivo. Exp Physiol 2005; 90: 53-9.
76. Silletti S, Yebra M, Perez B, Cirulli V, McMahon M, Montgomery AM. Extracellular signal-regulated kinase (ERK)-dependent gene expression contributes to L1 cell adhesion molecule-dependent motility and invasion. J Biol Chem 2004; 279: 28880-8.
77. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci 2004; 5: 146-56.
78. Spencer T, Filbin MT. A role for cAMP in regeneration of the adult mammalian CNS. J Anat 2004; 204: 49-55.
79. Staugaitis SM, Smith PR, Colman DR. Expression of myelin basic protein isoforms in nonglial cells. J Cell Biol 1990; 110: 1719-27.
80. Thuret S, Moon LDF, Gage F. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 2006; 7: 628-43.
81. Tiunova A, Anokhin KV, Schachner M, Rose SP. Three time windows for amnestic effect of antibodies to cell adhesion molecule L1 in chicks. Neuroreport 1998; 9: 1645-8.
82. Uemura T, Shepherd S, Ackerman L, Jan LY, Jan YN. Numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 1989; 58: 349-60.
83. Venero C, Tilling T, Hermans-Borgmeyer I, Herrero AI, Schachner M, Sandi C. Water maze learning and forebrain mRNA expression of the neural cell adhesion molecule L1. J Neurosci Res 2004; 75: 172-81.
84. Viala D, Buser P. The effects of DOPA and 5-HT on rhythmic efferent discharges in hind limb nerves in the rabbit. Brain Res 1969; 12: 437-43.
85. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK. Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 2000; 149: 263-70.
86. Wang X, Messing A, David S. Axonal and nonneuronal cell responses to spinal cord injury in mice lacking glial fibrillary acidic protein. Exp Neurol 1997; 148: 568-76.
87. Wood P, Moya F, Eldridge C, Owens G, Ranscht B, Schachner M, et al. Studies of the initiation of myelination by Schwann cells. Ann N Y Acad Sci 1990; 605: 1-14.
88. Xu G, Nie DY, Wang WZ, Zhang PH, Shen J, Ang BT, et al. Optic nerve regeneration in polyglycolic acid-chitosan conduits coated with recombinant L1-Fc. Neuroreport 2004; 15: 2167-72.
89. Xu K, Malouf AT, Messing A, Silver J. Glial fibrillary acidic protein is necessary for mature astrocytes to react to beta-amyloid. Glia 1999; 25: 390-403.
90. Yip PM, Zhao X, Montgomery AM, Siu CH. The Arg-Gly-Asp motif in the cell adhesion molecule L1 promotes neurite outgrowth via interaction with the alphavbeta3 integrin. Mol Biol Cell 1998; 9: 277-90.
91. Yiu G, He Z. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 2006; 7: 617-27.
92. Zhang Y, Bo X, Schoepfer R, Holtmaat AJ, Verhaagen J, Emson PC, et al. 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: 14883-8.