Schwann cell transplantation for repair of the adult spinal cord

Journal of Neurotrauma

Volumn 23, Issue 3-4, 2006, Pages 453-467

  Oudega, Martin ^a,b   Xu, Xiao Ming ^c  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of Louisville School of Medicine   (United States)

Author keywords

cAMP; Central nervous system; Endogenous repair; Glial scar; Neurotrophins; Olfactory ensheathing glia; Peripheral nerve; Schwann cell culture; Spinal cord injury

Indexed keywords

CYCLIC AMP; NEUROTROPHIN;

ANIMAL EXPERIMENT; ASTROCYTE; AUTOTRANSPLANTATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSPLANTATION; MYELINATION; NERVE FIBER REGENERATION; NERVE FUNCTION; NERVE GRAFT; NERVE REGENERATION; NONHUMAN; OLIGODENDROGLIA; REVIEW; SCAR; SCHWANN CELL; SPINAL CORD INJURY;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSPLANTATION; COMBINED MODALITY THERAPY; HUMANS; NEUROGLIA; PERIPHERAL NERVES; SCHWANN CELLS; SPINAL CORD INJURIES;

EID: 33646560612     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.23.453     Document Type: Review

References (123)

1. ACHESON, A., BARKER, P.A., ALDERSON, R.F., MILLER, F.D., and MURPHY, R.A. (1991). Detection of brain-derived neurotrophic factor-like activity in fibroblasts and Schwann cells: inhibition by antibodies to NGF. Neuron 7, 265-275.
2. AGUAYO, A.J., EPPS, J., CHARRON, L., and BRAY, G.M. (1976). Multipotentiality of Schwann cells in cross-anastomosed and grafted myelinated and unmyelinated nerves: quantitative microscopy and radioautography. Brain Res. 104, 1-20.
3. ALLT, G. (1975). The node of Ranvier in experimental allergic neuritis: an electron microscope study. J. Neurocytol. 4, 63-76.
4. ARD, M.D., BUNGE, R.P., and BUNGE, M.B. (1987). Comparison of the Schwann cell surface and Schwann cell extracellular matrix as promoters of neurite growth. J. Neurocytol. 16, 539-555.
5. ARENAS, E., and PERSSON, H. (1994). Neurotrophin-3 prevents the death of adult central noradrenergic neurons in vivo. Nature 367, 368-371.
6. ASKANAS, V., ENGEL, W.K., DALAKAS, M.C., LAWRENCE, J.V., and CARTER, L.S. (1980). Human Schwann cells in tissue culture: histochemical and ultrastructural studies. Arch. Neurol. 37, 329-337.
7. BAICHWAL, R.R., BIGBEE, J.W., and DEVRIES, G.H. (1988). Macrophage-mediated myelin-related mitogenic factor for cultured Schwann cells. Proc. Natl. Acad. Sci. U.S.A. 85, 1701-1705.
8. BAMBER, N.I., LI, H., LU, X., OUDEGA, M., AEBISCHER, P., and XU, X.M. (2001) Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur. J. Neurosci. 13, 257-268.
9. BARNETT, S. (2004). Olfactory ensheathing cells: unique glial cell types? J. Neurotrauma 21, 375-382.
10. BARON-VAN EVERCOOREN, A. (1994). Future prospects in transplantation. Ann. Neurol. 36, S151-S156.
11. BARON-VAN EVERCOOREN, A., GANSMÜLLER, A., CLERIN, E., and GUMPEL, M. (1991). Hoechst 33342, a suitable marker for Schwann cells after transplantation in the mouse spinal cord. Neurosci. Lett. 131, 241-244.
12. BARON-VAN EVERCOOREN, A., DUHAMEL-CLERIN, E., BOUTRY, J.M., HAUW, J.J., and GUMPEL, M. (1993). Pathways of migration of transplanted Schwann cells in the demyelinated mouse spinal cord. J. Neurosci. Res. 35, 428-138.
13. BEATTIE, M.S., BRESNAHAN, J.C., KOMON, J., et al. (1997). Endogenous repair after spinal cord contusion injuries in the rat. Exp. Neurol. 148, 453-463.
14. BIXBY, J.L., LILIEN, J., and REICHARDT, L.F. (1988). Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J. Cell Biol. 107, 353-361.
15. BLAKEMORE, W.F. (1975). Remyelination by Schwann cells of axons demyelinated by intraspinal injection of 6-aminonicotinamide in the rat. J. Neurocytol. 4, 745-757.
16. BLAKEMORE, W.F. (1977). Remyelination of CNS axons by Schwann cells transplanted from the sciatic nerve. Nature 266, 68-69.
17. BLIGHT, A.R., and YOUNG, W. (1989). Central axons in injured cat spinal cord recover electrophysiological function following remyelination by Schwann cells. J. Neurol. Sci. 91, 15-34.
18. BLITS, B., DIJKHUIZEN, P.A., BOER, G.J., and VERHAAGEN, J. (2000). Intercostal nerve implants transduced with an adenoviral vector encoding neurotrophin-3 promote regrowth of injured rat corticospinal tract fibers and improve hindlimb function. Exp. Neurol. 164, 25-37.
19. BOZYCZKO, D., and HORWITZ, A.F. (1986). The participation of a putative cell surface receptor for laminin and fibronectin in peripheral neurite extension. J. Neurosci. 6, 1241-1251.
20. BRADBURY, E.J., MOON, L.D.F., POPAT, R.J., et al. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640.
21. BRESNAHAN, J.C. (1978). An electron-microscopic analysis of axonal alterations following blunt contusion of the spinal cord of the rhesus monkey (Macaca, mulatta). J. Neurol. Sci. 37, 59-82.
22. BROCKES, J.P., FIELDS, K.L., and RAFF, M.C. (1979). Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res. 165, 105-118.
23. BROCKES, J.P., LEMKE, G.E., and BALZER, D.R., JR. (1980). Purification and preliminary characterization of a glial growth factor from the bovine pituitary. J. Biol. Chem. 255, 8374-8377.
24. BUNGE, R.P. (1994). Clinical implications of recent advances in neurotrauma research, in: The Neurobiology of CNS Trauma. S.A. Salzman, and A.I. Faden (eds), Oxford University Press, New York, pps. 329-339.
25. BUNGE, M.B., and PEARSE, D.D. (2003). Transplantation strategies to promote repair of the injured spinal cord. J. Rehabil. Res. Dev. 40, 55-62.
26. BUNGE, M.B., HOLETS, V.R., BATES, M.L., CLARKE, T.S., and WATSON, B.D. (1994). Characterization of photochemically induced spinal cord injury in the rat by light and electron microscopy. Exp. Neurol. 127, 76-93.
27. CAI, D., QIU, J., CAO, Z., McATEE, M., BREGMAN, B.S., and FILBIN, M.T. (2001). Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J. Neurosci. 21, 4731-4739.
28. CASELLA, G.T., BUNGE, R.P., and WOOD, P.M. (1996). Improved method for harvesting human Schwann cells from mature peripheral nerve and expansion in vitro. Glia 17, 327-338.
29. CHAU, C.H., SHUM, D.K.Y., and XU, X.-M. (2004a). Combinatorial strategies towards spinal cord repair: enhancement of the Schwann cell bridge and modification of the graft-host interface. Preclinica 2, 409-415.
30. CHAU, C.H., SHUM, D.K., LI, H., et al. (2004b). Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J. 18, 194-196.
31. CHENG, H., CAO, Y., and OLSON, L. (1996). Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273, 510-513.
32. CORNBROOKS, C.J., CAREY, D.J., McDONALD, J.A., TIMPL, R., and BUNGE, R.P. (1983). In vivo and in vitro observations on laminin production by Schwann cells. Proc. Natl. Acad. Sci. U.S.A. 80, 3850-3854.
33. DANILOFF, J.K., LEVI, G., GRUMET, M., RIEGER, F., and EDELMAN, G.M. (1986). Altered expression of neuronal cell adhesion molecules induced by nerve injury and repair. J. Cell Biol. 103(3), 929-945.
34. DAVID, S., and AGUAYO, A.J. (1981). Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933.
35. DAVIES, S.J.A., GOUCHER, D.R., DULLER, C., and SILVER, J. (1999). Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 19, 5810-5822.
36. DONG, Z., BRENNAN, A., LIU, N., et al. (1995). Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15, 585-596.
37. DUPIN, E., BAROFFIO, A., DULAC, C., CAMERON-CURRY, P., and LE DOUARIN, N.M. (1990). Schwann-cell differentiation in clonal cultures of the neural crest, as evidenced by the anti-Schwann cell myelin protein monoclonal antibody. Proc. Natl. Acad. Sci. U.S.A. 87, 1119-1123.
38. EVANS, P.D., REALE, V., and VILLEGAS, J. (1985). The role of cyclic nucleotides in modulation of the membrane potential of the Schwann cell of squid giant nerve fibre. J. Physiol. 363, 151-167.
39. FAULKNER, J.R., HERRMANN, J.E., WOO, M.J., TANSEY, K.E., DOAN, N.B., and SOFRONIEW, M.V. (2004). Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 24, 2143-2155.
40. FAWCETT, J.W., and ASHER, R.A. (1999). The glial scar and central nervous system repair. Brain Res. Bull. 49, 377-391.
41. FEIGIN, I., and OGATA, J. (1971). Schwann cells and peripheral myelin within human central nervous tissues: the mesenchymal character of Schwann cells. J. Neuropathol. Exp. Neurol. 30, 603-612.
42. FELTRI, M.L., SCHERER, S.S., WRABETZ, L., KAMHOLZ, J., and SHY, M.E. (1992). Mitogen-expanded Schwann cells retain the capacity to myelinate regenerating axons after transplantation into rat sciatic nerve. Proc. Natl. Acad. Sci. U.S.A. 89, 8827-8831.
43. FELTS, P.A., and SMITH, K.J. (1992). Conduction properties of central nerve fibers remyelinated by Schwann cells. Brain Res. 574, 178-192.
44. GALLI, C., LAGUTINA, I., and LAZZARI, G. (2003). Introduction to cloning by nuclear transplantation. Cloning Stem Cells 5, 223-232.
45. GANSMULLER, A., PASCAL, F., DUHAMEL, E., et al. (1992). Photoconversion of carbocyanine allows direct visualisation of transplanted glial cells by electron microscopy. Neurosci. Lett. 147, 151-154.
46. GIEHL, K.M., and TETZLAFF, W. (1996). BDNF and NT-3, but not NGF, prevent axotomy-induced death of rat corticospinal neurons in vivo. Eur. J. Neurosci. 8, 1167-1175.
47. GILMORE, S.A. (1971). Autoradiographic studies of intramedullary Schwann cells in irradiated spinal cords of immature rats. Anat. Rec. 171, 517-528.
48. GILMORE, S.A., and DUNCAN, D. (1968). On the presence of peripheral-like nervous and connective tissue within irradiated spinal cord. Anat. Rec. 160, 675-690.
49. HADLOCK, T.A., HEATON, J., CHENEY, M., and MACKINNON, S.E. (2005). Functional recovery after facial and sciatic nerve crush injury in the rat. Arch. Facial Plast. Surg. 7, 17-20.
50. HASAN, N.A., NEUMANN, M.M., DE SOUKY, M.A., SO, K.P., and BEDI, K.S. (1996). The influence of predegenerated nerve grafts on axonal regeneration from prelesioned peripheral nerves. J. Anat. 189, 293-302.
51. HENDRIKS, W.T., RUITENBERG, M.J., BLITS, B., BOER, G.J., and VERHAAGEN, J. (2004). Viral vector-mediated gene transfer of neurotrophins to promote regeneration of the injured spinal cord. Prog. Brain Res. 146, 451-476.
52. HEUMANN, R., LINDHOLM, D., BANDTLOW, C., et al. (1987). Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc. Natl. Acad. Sci. U.S.A. 84, 8735-8739.
53. HIRANO, A., ZIMMERMAN, H.M., and LEVINE, S. (1969). Electron microscopic observations of peripheral myelin in a central nervous system lesion. Acta Neuropathol. (Berl.) 12, 348-365.
54. HOUWELING, D.A., LANKHORST, A.J., GISPEN, W.H., BAR, P.R., and JOOSTEN, E.A. (1998). Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery. Exp. Neurol. 153, 49-59.
55. IANNOTTI, C., ZHANG, Y.P., SHIELDS, C.B., HAN, Y., BURKE, D.A., and XU, X.-M. (2004). A neuroprotective role for glial cell line-derived neurotrophic factor following moderate spinal cord contusion injury. Exp. Neurol. 189, 317-332.
56. IMAIZUMI, T., LANKFORD, K.L., and KOCSIS, J.D. (2000). Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res. 854, 70-78.
57. JAKEMAN, L.B., WEI, P., GUAN, Z., and STOKES, B.T. (1998). Brain-derived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury. Exp. Neurol. 154, 170-184.
58. KLEITMAN, N., SIMON, D.K., SCHACHNER, M., and BUNGE, R.P. (1988). Growth of embryonic retinal neurites elicited by contact with Schwann cell surfaces is blocked by antibodies to L1. Exp. Neurol. 102, 298-306.
59. KROMER, L.F., and CORNBROOKS, C.J. (1985). Transplants of Schwann cell cultures promote axonal regeneration in the adult mammalian brain. Proc. Natl. Acad. Sci. U.S.A. 82, 6330-6334.
60. LAKATOS, A., FRANKLIN, R.J., and BARNETT, S.C. (2000). Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 32, 214-225.
61. LAKATOS, A., BARNETT, S.C., and FRANKLIN, R.J. (2003a). Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp. Neurol. 184, 237-246.
62. LAKATOS, A., SMITH, P.M., BARNETT, S.C., and FRANKLIN, R.J. (2003b). Meningeal cells enhance limited CNS remyelination by transplanted olfactory ensheathing cells. Brain 126, 598-609.
63. LEE, Y.S., HSIAO, I., and LIN, V.W. (2002). Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J. Neurotrauma 19, 1203-1216.
64. LEE, Y.S., LIN, C.Y., ROBERTSON, R.T., HSIAO, I., and LIN, V.W. (2004). Motor recovery and anatomical evidence of axonal regrowth in spinal cord-repaired adult rats. J. Neuropathol. Exp. Neurol. 63, 233-245.
65. LEMONS, M.L., HOWLAND, D.R., and ANDERSON, D.K. (1999). Chondroitin sulfate proteoglycan immunoreactivity increases following spinal cord injury and transplantation. Exp. Neurol. 160, 51-65.
66. LI, L., FIELD, P.M., and RAISMAN, G. (1997). Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277, 2000-2002.
67. MARTINI, R., and SCHACHNER, M. (1988). Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and myelin-associated glycoprotein) in regenerating adult mouse sciatic nerve. J. Cell Biol. 106, 1735-1746.
68. McKEON, R.J., SCHREIBER, R.C., RUDGE, J.S., and SILVER, J. (1991). Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J. Neurosci. 11, 3398-3411.
69. MENEI, P., MONTERO-MENEI, C., WHITTEMORE, S.R., BUNGE, R.P., and BUNGE, M.B. (1998). Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. Eur. J. Neurosci. 10, 607-621.
70. MEYER, M., MATSUOKA, I., WETMORE, C., OLSON, L., and THOENEN, H. (1992). Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J. Cell Biol. 119, 45-54.
71. MING, G.L., SONG, H.J., BERNINGER, B., HOLT, C.E., TESSIER-LAVIGNE, M., and POO, M.M. (1997). cAMP-dependent growth cone guidance by netrin-1. Neuron 19, 1225-1235.
72. MIRSKY, R., and JESSEN, K.R. (1996). Schwann cell development, differentiation and myelination. Curr. Opin. Neurobiol. 6, 89-96.
73. MIRSKY, R., JESSEN, K.R., BRENNAN, A., et al. (2002). Schwann cells as regulators of nerve development. J. Physiol. Paris 96, 17-24.
74. MOON, L.D., ASHER, R.A., RHODES, K.E., and FAWCETT, J.W. (2001). Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 4, 465-466.
75. MOON, L.D., ASHER, R.A., RHODES, K.E., and FAWCETT, J.W. (2002). Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience 109, 101-117.
76. MORRISSEY, T.K., KLEITMAN, N., and BUNGE, R.P. (1991). Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J. Neurosci. 11, 2433-2442.
77. MYCKATYN, T.M., and MACKINNON, S.E. (2004). A review of research endeavors to optimize peripheral nerve reconstruction. Neurol. Res. 26, 124-138.
78. NAKAHARA, Y., GAGE, F.H., and TUSZYNSKI, M.H. (1996). Grafts of fibroblasts genetically modified to secrete NGF, BDNF, NT-3, or basic FGF elicit differential responses in the adult spinal cord. Cell Transplant 5, 191-204.
79. NEUBERGER, T.J., and DE VRIES, G.H. (1993). Distribution of fibroblast growth factor in cultured dorsal root ganglion neurons and Schwann cells. II. Redistribution after neural injury. J. Neurocytol. 22, 449-460.
80. NEUMANN, S., BRADKE, F., LESSIER-LAVIGUE, M., and BASBAUM, A.I. (2002). Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885-893.
81. NIKULINA, E., TIDWELL, J.L., DAI, H.N., BREGMAN, B.S., and FILBIN, M.T. (2004). The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc. Natl. Acad. Sci. U.S.A. 101, 8786-8790.
82. NORENBERG, M.D., SMITH, J., and MARCILLO, A. (2003). The pathology of human spinal cord injury: defining the problems. J. Neurotrauma 21, 429-440.
83. OFFENHAUSER, N., BOHM-MATTHAEI, R., TSOULFAS, P., PARADA, L., and MEYER, M. (1995). Developmental regulation of full-length trkC in the rat sciatic nerve. Eur. J. Neurosci. 7, 917-925.
84. [Erratumin: Eur. J. Neurosci. 7, 2005.]
85. ONIFER; S.M., MAGNUSON, D.S.K., SHIELDS, C.B., and WHITTEMORE, S.R. (2000). Grafting into the injured spinal cord to restore locomotion: two decades of promise yet to be fufilled. Neurosci. News 3, 50-58.
86. OUDEGA, M., and HAGG, T. (1996). Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp. Neurol. 140, 218-229.
87. OUDEGA, M., and HAGG, T. (1999). Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res. 818, 431-138.
88. OUDEGA, M., VARON, S., and HAGG, T. (1994). Regeneration of adult rat sensory axons into intraspinal nerve grafts: promoting effects of conditioning lesion and graft predegeneration. Exp. Neurol. 129, 194-206.
89. OUDEGA, M., MOON, L.D., and DE ALMEIDA LEME, R.J. (2005). Schwann cells for spinal cord repair. Braz. J. Med. Biol. Res. 38, 825-835.
90. OWENS, G.G., and BUNGE, R.P. (1991). Schwann cells infected with a recombinant retrovirus expressing myelin-associated glycoprotein antisense RNA do not form myelin. Neuron 7, 565-575.
91. PARMANTIER, E., LYNN, B., LAWSON, D., et al. (1999). Schwann cell-derived Desert hedgehog controls the development of peripheral nerve sheaths. Neuron 23, 713-724.
92. PEARSE, D.D., BLITS, B., BUNGE, M.B., et al. (2004a). Minimally invasive strategies for administration of genetically-modified glia in the contused spinal cord. Mol. Therapy. 9, S197.
93. PEARSE, D.D., PEREIRA, F.C., MARCILLO, A.E., et al. (2004b). cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat. Med. 10, 610-616.
94. PINZON, A., CALANCIE, B., OUDEGA, M., and NOGA, B.R. (2001). Conduction of impulses by axons regenerated in a Schwann cell graft in the transected adult rat thoracic spinal cord. J. Neurosci. Res. 64, 533-541.
95. PLANT, G.W., BATES, M.L., and BUNGE, M.B. (2001). Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-trasected spinal cord interface. Mol. Cell. Neurosci. 17, 471-187.
96. PLANT, G.W., CURRIER, P.P., CUERVO, E.P., et al. (2002). Purified adult ensheathing glia fail to myelinate axons under culture conditions that enable Schwann cells to form myelin. J. Neurosci. 22, 6083-6091.
97. PORTER, S., CLARK, M.B., GLASER, L., and BUNGE, R.P. (1986). Schwann cells stimulated to proliferate in the absence of neurons retain full functional capability. J. Neurosci. 6, 3070-3078.
98. RAFF, M.C., HORNBY-SMITH, A., and BROCKES, J.P. (1978). Cyclic AMP as a mitogenic signal for cultured rat Schwann cells. Nature 273, 672-673.
99. RAINE, C.S. (1976). On the occurrence of Schwann cells within the normal central nervous system, J. Neurocytol. 5, 371-380.
100. RAISMAN, G. (1997). Use of Schwann cells to induce repair of adult CNS tracts. Rev. Neurol. (Paris) 153, 521-525.
101. RAMON-CUETO, A., and NIETO-SAMPEDRO, M. (1994). Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp. Neurol. 127, 232-244.
102. RAMON-CUETO, A., PLANT, G.W., AVILA, J., and BUNGE, M.B. (1998). Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci. 18, 3803-3815.
103. RAMON-CUETO, A., CORDERO, M.I., SANTOS-BENITO, F.F., and AVILA, J. (2000). Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25, 425-435.
104. RAMON Y CAJAL, S. (1928). Degeneration and Regeneration of the Nervous System (R.M. May, trans). Oxford University Press: London.
105. RENDE, M., MUIR, D., RUOSLAHTI, E., HAGG, T., VARON, S., and MANTHORPE, M. (1992). Immunolocalization of ciliary neuronotrophic factor in adult rat sciatic nerve. Glia 5, 25-32.
106. RICHARDSON, P.M., and ISSA, V.M. (1984). Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309, 791-793.
107. RICHARDSON, P.M., McGUINNESS, U.M., and AGUAYO, A.J. (1980). Axons from CNS neurons regenerate into PNS grafts. Nature 284, 264-265.
108. SALZER, J.L. (2002). Nodes of Ranvier come of age. Trends Neurosci. 25, 2-5.
109. SALZER, J.L., and BUNGE, R.P. (1980). Studies of Schwann cell proliferation. I. An analysis in tissue culture of proliferation during development, Wallerian degeneration, and direct injury. J. Cell Biol. 84, 739-752.
110. SCARPINI, E., KREIDER, B.Q., LISAK, R.P., and PLEASURE, D.E. (1988). Establishment of Schwann cell cultures from adult rat peripheral nerves. Exp. Neurol. 102, 167-176.
111. SCHNELL, L., SCHNEIDER, R., KOLBECK, R., BARDE, Y.-A., and SCHWAB, M.E. (1994). Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173.
112. SONG, H.J., MING, G.L., and POO, M.M. (1997). cAMP-induced switching in turning direction of nerve growth cones. Nature 388, 275-279.
113. SPRINGER, J.E., MU, X., BERGMANN, L.W., and TROJANOWSKI, J.Q. (1994). Expression of GDNF mRNA in rat and human nervous tissue. Exp. Neurol. 127, 167-170.
114. TAKAMI, T., OUDEGA, M., BATES, M.L., WOOD, P.M., KLEITMAN, N., and BUNGE, M.B. (2002). Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J. Neurosci. 22, 6670-6681.
115. TOHILL, M.P., MANTOVANI, C., MANN, D., WIBER, G.M., and TERENGHI, G. (2002). GFP-labeled Schwann cells for the study of bioengineered cellular nerve grafts. Eur. Cell Mater. 4, Suppl. 2, 45.
116. TUSZYNSKI, M.H., WEIDNER, N., McCORMACK, M., MILLER, I., POWELL, H., and CONNER, J. (1998). Grafts of genetically modified Schwann cells to the spinal cord: survival, axon growth, and myelination. Cell Transplant. 7, 187-196.
117. TZAKOS, A.G., TROGANIS, A., THEODOROU, V., et al. (2005). Structure and function of the myelin proteins: current status and perspectives in relation to multiple sclerosis. Curr. Med. Chem. 12, 1569-1587.
118. WILKINS, P.L., SUCHOVSKY, D., and BERTI-MATTERA, L.N. (1997). Immortalized Schwann cells express endothelin receptors coupled to adenylyl cyclase and phospholipase C. Neurochem. Res. 22, 409-418.
119. WOOD, P.M. (1976). Separation of functional Schwann cells and neurons from normal peripheral nerve tissue. Brain Res. 115, 361-375.
120. XU, X.M., GUENARD, V., KLEITMAN, N., and BUNGE, M.B. (1995a). Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 351, 145-160.
121. XU, X.M., GUENARD, V., KLEITMAN, N., AEBISCHER, P., and BUNGE, M.B. (1995b). A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 134, 261-272.
122. XU, X.M., CHEN, A., GUENARD, V., KLEITMAN, N., and BUNGE, M.B. (1997). Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J. Neurocytol. 26, 1-16.
123. YE, J.-H., and HOULE, J.D. (1997). Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143, 70-81.