Repair of chronic spinal cord injury

Experimental Neurology

Volumn 182, Issue 2, 2003, Pages 247-260

  Houle, John D ^a   Tessler, Alan ^b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

CNS; Neurotrophic factor; Regeneration; Spinal cord; Transplantation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; BICUCULLINE; CILIARY NEUROTROPHIC FACTOR; CYTOSKELETON PROTEIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLYCINE RECEPTOR ANTAGONIST; NEUROFILAMENT PROTEIN; NEUROMODULIN; NEUROTRANSMITTER; STRYCHNINE;

CHRONIC DISEASE; DENERVATION; EXERCISE; HUMAN; METABOLIC DISORDER; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE TRANSPLANTATION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROGNOSIS; REVIEW; SPINAL CORD INJURY; TREATMENT FAILURE;

EID: 0041700229     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00029-3     Document Type: Review

References (150)

1. Aguayo A.J., David S., Richardson P., Bray G.M. Axonal elongation in peripheral and central nervous system transplants. Adv. Cell. Neurobiol. 3:1979;215-234.
2. Åkesson E., Holmberg L., Jönhagen M.E., Kjældgaard A., Falci S., Sundtröm E., Seiger Å. Solid human embryonic spinal cord xenografts in acute and chronic spinal cord cavities a morphological and functional study . Exp. Neurol. 170:2001;305-316.
3. Akiyama Y., Radtke C., Kocsis J.D. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J. Neurosci. 22:2002;6623-6630.
4. Bandtlow C.E., Schwab M.E. NI-35/250/Nogo-a a neurite growth inhibitor restricting structural plasticity and regeneration of nerve fibers in the adult vertebrate CNS . Glia. 29:2000;175-181.
5. Barbeau H., Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res. 412:1987;84-95.
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. 546:1991;250-260.
7. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma. 12:1995;1-21.
8. Beattie M.S., Bresnahan J.C. Cell death, repair and recovery of function after spinal cord contusion injuries in rats. Kalb R., Strittmater S.M. Neurobiology of spinal cord injury. 2000;1-22 Humana Press, Totowa, NJ.
9. Beattie M.S., Bresnahan J.C., Komon J., Tovar C.A., Van Meter M., Anderson D.K., Faden A.I., Hsu C.Y., Noble L.J., Salzman S., Young W. Endogenous repair after spinal cord contusion injuries in the rat. Exp. Neurol. 148:1997;453-463.
10. Beattie M.S., Li Q., Bresnahan J.C. Cell death and plasticity after experimental spinal cord injury. Prog. Brain Res. 128:2000;9-21.
11. Behar O., Mizuno K., Neumann S., Woolf C.J. Putting the spinal cord together again. Neuron. 26:2000;291-293.
12. Benfey M., Aguayo A.J. Extensive elongation of axons from rat brain into peripheral nerve grafts. Nature. 296:1982;150-152.
13. Benowitz L.I., Goldberg D.E., Madsen J.R., Soni D., Irwin N. Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proc. Natl. Acad. Sci. USA. 96:1999;13486-13490.
14. Bjugn R., Nyengaard J.R., Rosland J.H. Spinal cord transection - no loss of distal ventral horn neurons. Exp. Neurol. 148:1997;179-186.
15. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Pate P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 416:2002;589-590.
16. Bregman B.S. Recovery of function after spinal cord injury transplantation strategies . Dunnett S.B., Bjorklund A. Functional Neural Transplantation. 1994;489-529 Raven Press, Ltd, New York, NY.
17. Bregman B.S. Regeneration in the spinal cord. Curr. Opin. Neurobiol. 8:1998;800-807.
18. Bregman B.S., McAtee M., Dai H.N., Kuhn P.L. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp. Neurol. 148:1997;475-494.
19. Bregman B.S., Reier P.J. Neural tissue transplants rescue axotomized rubrospinal cells from retrograde death. J. Comp. Neurol. 244:1986;86-95.
20. Bunge M.B. Bridging areas of injury in the spinal cord. The Neuroscientist. 7:2001;325-339.
21. Bunge R.P., Puckett W.R., Becerra J.L., Marcillo A., Quencer R.M. Observations on the pathology of human SCI - a review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv. Neurol. 59:1993;75-90.
22. Caroni P., Schwab M.E. Antibody against myelin-associated inhibitor of neurite growth neutralizes non-permissive substrate properties of CNS white matter. Neuron. 1:1988;85-96.
23. Carter D.A., Bray G.M., Aguayo A.J. Regenerated retinal ganglion cell axons can form well-differentiated synapses in the superior colliculus of adult hamsters. J. Neurosci. 9:1989;4042-4050.
24. Ceresa B.P., Schmid S.L. Regulation of signal transduction by endocytosis. Curr. Opin. Cell Biol. 12:2000;204-210.
25. Chau C., Barbeau H., Rossignol S. Early locomotor training with clonidine in spinal cats. J. Neurophysiol. 79:1998;392-409.
26. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ F., Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature. 403:2000;434-441.
27. Chen X.Y., Wolpaw J.R. Probable corticospinal tract control of spinal cord plasticity in the rat. J. Neurophysiol. 87:2001;645-652.
28. Coumans J.V., Lin T.T.-S., Dai H.N., MacArthur L., McAtee M., Nash C., Bregman B.S. Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J. Neurosci. 21:2001;9334-9344.
29. Das G.D. Neural transplantation in the spinal cord of adult rats. Conditions, survival, cytology and connectivity of the transplants. J. Neurosci. Res. 62:1983;191-210.
30. David S., Aguayo A.J. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science. 214:1981;931-933.
31. David S., Ousman S.S. Recruiting the immune response to promote axon regeneration in the injured spinal cord. The Neuroscientist. 8:2002;33-41.
32. Davies S.J.A., Goucher D.R., Doller C., Silver J. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 19:1999;5810-5822.
33. de Leon R.D., Roy R.R., Edgerton V.R. Is the recovery of stepping following spinal cord injury mediated by modifying existing neural pathways or by generating new pathways? A perspective. Phys. Ther. 81:2001;1904-1911.
34. DeVivo M.J. Epidemiology of traumatic spinal cord injury. Kirshblum S., Campagnolo D.I., DeLisa J.A. Spinal Cord Medicine. 2002;69-81 Lippincott Williams & Wilkins, Philadelphia.
35. Ditunno J.F. Jr., Formal C.S. Chronic spinal cord injury. N. Engl. J. Med. 330:1994;550-556.
36. Edgerton V.R., de Leon R.D., Harkema S.J., Hodgson J.A., London N., Reinkensmeyer D.J., Roy R.R., Talmadge R.J., Tillakaratne N.J., Timoszyk W., Tobin A. Retraining the injured spinal cord. J. Physiol. 533:2001;15-22.
37. Edgerton V.R., Roy R.R., Hodgson J.A., Gregor R.J., De Guzman C.P. Recovery of full weight-supporting locomotion of the hindlimbs after complete thoracic spinalization of adult and neonatal cats. Wernig A. Restorative Neurology, Plasticity of Motoneuronal Connection. 1991;405-418 Elsevier Publishers, New York, NY.
38. Emery E., Aldana P., Bunge M.B., Puckett W., Srinivasan A., Keane R.W., Bethea J., Levi A.D.O. Apoptosis after traumatic human spinal cord injury. J. Neurosurg. 89:1998;911-920.
39. Fawcett J.W. Astrocytic and neuronal factors affecting axon regeneration in the damaged central nervous system. Cell Tissue Res. 290:1997;371-377.
40. Feraboli-Lohnherr D., Orsal D., Yakovleff A., Giménez y Ribotta M., Privat A. Recovery of locomotor activity in the adult chronic spinal rat after sublesional transplantation of embryonic nervous cells specific role of serotonergic neurons . Exp. Brain Res. 113:1997;443-454.
41. Fernandes K.J.L., Tetzlaff W.G. Gene expression in axotomized neurons identifying the intrinsic determinants of axonal growth . Ingoglia N.A., Murray M. Axonal Regeneration in the Central Nervous System. 2001;219-266 Marcel Dekker, Inc, New York, NY.
42. Fitch M.T., Doller C., Combs C.K., Landreth G.E., Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma . J. Neurosci. 19:1999;8182-8198.
43. Frisen J., Verge V.M.K., Fried K., Reisling M., Persson H., Trotter J., Hökfelt T., Lindholm D. Characterization of glial trkB receptors differential response to injury in the central and peripheral nervous systems . Proc. Natl. Acad. Sci. USA. 90:1993;4971-4975.
44. Fu S.Y., Gordon T. Contributing factors to poor functional recovery after delayed nerve repair prolonged denervation . J. Neurosci. 15:1995;3886-3895.
45. Fu S.Y., Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 14:1997;67-116.
46. Geller H.M., Fawcett J.W. Building a bridge engineering spinal cord repair . Exp. Neurol. 174:2002;125-136.
47. Giménez y Ribotta M., 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. 201:2000;5144-5152.
48. Gordon T., Fu S. Long-term response to nerve injury. Seil F.J. Adv. Neurol., Neuronal Regeneration, Reorganization and Repair. 1997;185-199 Lippincott-Raven, Philadelphia.
49. GranPre T., Nakamura F., Vartanian T., Strittmatter S.M. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature. 403:2000;439-444.
50. Grill R.A., Blesch A., Tuszynski M.H. Robust growth of chronically injured spinal cord axons induced by grafts of genetically-modified NGF-secreting cells. Exp. Neurol. 148:1997;444-452.
51. Guttmann L. Spinal Cord Injuries. 1976;731 Blackwell Scientific Publications, Oxford, UK.
52. Hill C.E., Beattie M.S., Bresnahan J.C. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp. Neurol. 171:2001;153-169.
53. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El Manira A., Prockop D.J., Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. USA. 99:2002;2199-2204.
54. Hoke A., Gordon T., Zochodne D.W., Sulaiman O.A. A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp. Neurol. 173:2002;77-85.
55. Horner P.J., Gage F.H. Regenerating the damaged central nervous system. Nature. 407:2000;963-970.
56. Houle J. The structural integrity of glial scar tissue associated with a chronic spinal cord lesion can be altered by transplanted fetal spinal cord tissue. J. Neurosci. Res. 31:1992;120-130.
57. Houle J.D. Demonstration of the potential for chronically injured neurons to regenerate axons into intraspinal peripheral nerve grafts. Exp. Neurol. 113:1991;1-9.
58. Houle, J.D., Eckenstein, F., 2002. Cytokine and neurotrophin mRNA expression with chronic injury and re-injury of the spinal cord. Soc. Neurosci. Abstr. 393.10.
59. Houle J.D., Jin Y. Chronically injured supraspinal neurons exhibit only modest axonal dieback in response to a cervical hemisection lesion. Exp. Neurol. 169:2001;208-217.
60. Houle J.D., Reier P.J. Transplantation of fetal spinal cord tissue into the chronically injured adult rat spinal cord. J. Comp. Neurol. 269:1988;535-547.
61. Houle J.D., Reier P.J. Regrowth of calcitonin gene-related peptide (CGRP) immunoreactive axons from the chronically injured rat spinal cord into fetal spinal cord tissue transplants. Neurosci. Lett. 103:1989;253-258.
62. Houle J.D., Schramm P., Herdegen T. Trophic factor modulation of c-Jun expression in supraspinal neurons after chronic spinal cord injury. Exp. Neurol. 154:1998;602-611.
63. Houle J.D., Skinner R.D., Garcia-Rill E., Turner K. Synaptic evoked potentials from regenerating dorsal root axons within fetal spinal cord tissue transplants. Exp. Neurol. 139:1996;278-290.
64. Houle J.D., Ye J.H. Changes occur in the ability to promote axonal regeneration as the post-injury period increases. NeuroReport. 8:1997;751-755.
65. Houle J.D., Ye J.H., Kane C.J.M. Axonal regeneration by chronically injured supraspinal neurons can be enhanced by exposure to insulin-like growth factor, basic fibroblast growth factor or transforming growth factor beta. Restor. Neurol. Neurosci. 10:1996;205-215.
66. Houle J.D., Ziegler M.K. Bridging a complete transection lesion of adult rat spinal cord with growth factor-treated nitrocellulose implants. J. Neural Transpl. Plasticity. 5:1994;115-124.
67. Huang D.W., McKerracher L., Braun P., David S. A therapeutic vaccine approach to stimulate axon regeneration in the adult mammalian spinal cord. Neuron. 24:1999;639-647.
68. Huber A.B., Weinmann O., Brösamie C., Oertle T., Schwab M.E. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J. Neurosci. 22:2002;3553-3567.
69. Hughes J.T. Pathology of the Spinal Cord. 1966;196 Lippincott, Philadelphia.
70. Ikeda O., Murakami M., Ino H., Yamazaki M., Nemoto T., Koda M., Nakayama C., Moriya H. Acute up-regulation of brain-derived neurotrophic factor expression resulting from experimentally induced injury in the rat spinal cord. Acta Neuropathal. 102:2001;239-245.
71. Itoh Y., Waldeck R.F., Tessler A., Pinter M.J. Regenerated dorsal root fibers form functional synapses in embryonic spinal cord transplants. J. Neurophysiol. 76:1996;1236-1245.
72. Jacob J., Hacker A., Guthrie S. Mechanisms and molecules in motor neuron specification and axon pathfinding. BioEssays. 23:2001;582-595.
73. Jakeman L., Reier P. Axonal projections between fetal spinal cord transplants and the adult rat spinal cord a neuroanatomical tracing study of local interactions . J. Comp. Neurol. 307:1991;311-334.
74. Jin Y., Tessler A., Fischer T., Houle J.D. Fibroblasts genetically modified to produce BDNF support regrowth of chronically injured serotonergic axons. Neurorehab. Neural Repair. 14:2000;311-317.
75. Jin Y., Tessler A., Fischer I., Houle J.D. Transplants of fibroblasts genetically modified to express BDNF promote axonal regeneration from supraspinal neurons following chronic spinal cord injury. Exp. Neurol. 177:2002;265-275.
76. Kaegi S., Schwab M.E., Dietz V., Fouad K. Electromyographic activity associated with spontaneous functional recovery after spinal cord injury in rats. Eur. J. Neurosci. 16:2002;249-258.
77. Kaelan C., Jacobsen P.F., Kakulas B.A. An investigation of possible transynaptic neuronal degeneration in human spinal cord injury. J. Neurol. Sci. 86:1988;231-237.
78. Kakulas B.A. The applied neuropathology of human spinal cord injury. Spinal Cord. 37:1999;79-88.
79. Kakulas B.A., Taylor J.R. Pathology of injuries of the vertebral column and spinal cord. Vinken P.J., Bruyn P.J., Klauwens H.L., Frankel H.L. Handbook of Clinical Neurology. Spinal Cord Trauma. 1992;21-51 Elsevier, Amsterdam.
80. Kierstead S.A., Rasminsky M.A., Fukuda Y., Carter D.A., Aguayo A.J., Vidal Sanz M. Electrophysiologic responses in hamster superior colliculus evoked by regenerating retinal axon. Science. 246:1989;255-257.
81. Kim D., Adipudi V., Shibayama M., Giszter S., Tessler A., Murray M., Simansky K.J. Direct agonists for serotonin receptors enhance locomotor function in rats that received neural transplants after neonatal spinal transection. J. Neurosci. 19:1999;6213-6224.
82. Kobayashi N.R., Fan D., Giehl K.M., Bedard A.M., Wiegand S.J., Tetzlaff W. BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and Tα1-tubulin mRNA expression and promote axonal regeneration. J. Neurosci. 17:1997;9583-9595.
83. Kwon B.W., Liu J., Messerer C., Kobayashi N.R., McGraw J., Oschipok L., Tetzlaff W. Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury. Proc. Natl. Acad. Sci. USA. 99:2002;3246-3251.
84. Kwon B.W., Liu J., Oschipok L., Tetzlaff W. Reaxotomy of chronically injured rubrospinal neurons results in only modest cell loss. Exp. Neurol. 177:2002;332-337.
85. Li Y., Field P.M., Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J. Neurosci. 18:1998;10514-10524.
86. Liebel D.J., Huang W., Young W., Parada L.F. Regulation of trk receptors following contusion of the rat spinal cord. Exp. Neurol. 167:2001;15-26.
87. Liu X.Z.X.M., Hu R., Du C., Zhang S.X., McDonald J.W., Dong H.X., Wu Y.J., Fan G.S., Jacquin M., Hsu C.Y., Choi D.W. Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17:1997;5395-5406.
88. Liu Y., Kim D., Himes B.T., Chow S.Y., Schallert T., Murray M., Tessler A., Fischer I. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rubrospinal axons and recovery of forelimb recovery. J. Neurosci. 19:1999;4370-4387.
89. Lovely R.G., Gregor R.J., Roy R.R., Edgerton V.R. Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cats. Brain Res. 514:1990;206-218.
90. Loy D.N., Talbott J.F., Onifer S.M., Mills M.D., Burke D.A., Dennison J.B., Fajardo L.C., Magnuson D.S., Whittemore S.R. Both dorsal and ventral spinal cord pathways contribute to overground locomotion in the adult rat. Exp. Neurol. 177:2002;575-580.
91. Lu J., Feron F., Mackay-Sim A., Waite P.M.E. Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain. 125:2002;14-21.
92. Magavi S.S., Leavitt B.R., Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature. 405:2000;951-954.
93. Magnuson D.S.K., Trinder T.C., Zhang Y.P., Burke D., Morassutti D.J., Shields C.B. Comparing deficits following excitotoxic and contusion injuries in the thoracic and lumbar spinal cord of the adult rat. Exp. Neurol. 156:1999;191-204.
94. McDonald J.W., Liu X.Z., Qu Y., Liu S., Mickey S.K., Turetsky D., Gottlieb D.I., Choi D.W. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nature Med. 5:1999;1410-1412.
95. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron. 13:1994;805-811.
96. Mukhopadhyay G., Doherty P., Walsh F.S., Crocker P.R., Filbin M.T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron. 13:1994;757-767.
97. Murray M., Fischer I. Transplantation and gene therapy combined approaches for repair of spinal cord injury . The Neuroscientist. 7:2001;28-41.
98. Nakamura M., Bregman B.S. Differences in neurotrophic factor gene expression profiles between neonate and adult rat spinal cord after injury. Exp. Neurol. 169:2001;407-415.
99. Nashmi R., Fehlings M.G. Changes in axonal physiology and morphology after chronic compressive injury of the rat thoracic spinal cord. Neuroscience. 104:2001;235-251.
100. Neumann S., Bradke F., Tessier-Lavigne M., Basbaum A.I. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron. 34:2002;885-893.
101. Neumann S., Woolf C.J. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron. 23:1999;83-91.
102. Niederost B.P., Zimmermann D.R., Schwab M.E., Bandtlow C.E. Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycan. J. Neurosci. 19:1999;8979-8989.
103. Novikova L.N., Novikov L.N., Kellerth I.-O. Survival effects of BDNF and NT-3 on axotomized rubrospinal neurons depend on the temporal pattern of neurotrophin administration. Eur. J. Neurosci. 12:2000;776-780.
104. Oudega M., Hagg T. Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res. 818:1999;431-438.
105. Oudega M., Vargas C.G., Weber A.B., Kleitman N., Bunge M.B. Long-term effects of methylprednisolone following transection of adult rat spinal cord. Eur. J. Neurosci. 11:1999;2453-2464.
106. Pallini R., Fernandez E., Sbriccoli A. Retrograde degeneration of corticospinal axons following transection of the spinal cord in rats. A quantitative study with anterogradely transported horseradish peroxidase. J. Neurosurg. 68:1988;124-128.
107. Pasterkamp R.J., Giger R.J., Ruitenberg M.J., Holtmaat A.J., De Wit J., De Winter F., Verhaagen J. Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol. Cell Neurosci. 13:1999;143-166.
108. Peterson C.A., Murphy R.J.L., Dupont-Versteegden E.E., Houle J.D. Cycling exercise and fetal spinal cord transplantation act synergistically on atrophied muscle following chronic spinal cord injury in rats. Neurorehab. Neural Repair. 14:2000;85-91.
109. Privat A., Mansour H., Rajaofetra N., Geffard M. Intraspinal transplants of serotonergic neurons in the adult rat. Br. Res. Bull. 22:1989;123-129.
110. Qiu J., Cai D., Dai H., McAtee M., Hoffman P.N., Bregman B.S., Filbin M.T. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron. 34:2002;895-903.
111. Raineteau O., Z'Graggen W.J., Thallmair M., Schwab M.E. Sprouting and regeneration after pyramidotomy and blockade of the myelin-associated neurite growth inhibitors NI-35/250 in adult rats. Eur. J. Neurosci. 11:1999;1486-1490.
112. Ramón-Cueto A., Plant G.W., Avila J., Bunge M.B. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci. 18:1998;3803-3815.
113. Ramón y Cajal S. Degeneration and Regeneration of the Nervous System. 1928;Oxford University Press, New York, NY.
114. Reeve C. Still Me. 1998;309 Random House, New York.
115. Reier P.J., Bregman B.S., Wujek J.R. Intraspinal transplantation of fetal spinal cord tissue an approach toward functional repair on the injured spinal cord . Goldberger M., Gorio A., Murray M. Proceedings of the International Symposium on Plasticity and Development of the Mammalian Spinal Cord. 1986;251-269 Liviana Press, Padova.
116. Reier P.J., Stokes B.T., Thompson F.J., Anderson D.K. Fetal cell grafts into resection and contusion/compression injuries of the rat and cat spinal cord. Exp. Neurol. 115:1992;177-188.
117. Reier P.J., Thompson F.J., Fessler R.G., Anderson D.K., Wirth E.D. III. Spinal cord injury and fetal CNS tissue transplantation an initial "bench to bedside" translational research experience . Ingoglia N.A., Murray M. Axonal Regeneration in the Central Nervous System. 2001;603-648 Marcel Dekker Inc, New York, NY.
118. Richardson P.M., McGuinness U.M., Aguayo A.J. Axons from CNS neurons regenerate into PNS grafts. Nature. 284:1980;264-265.
119. Robinson G.A., Goldberger M.E. The development and recovery of motor function in spinal cats. II. Pharmacological enhancement of recovery. Exp. Brain Res. 62:1986;387-400.
120. Rossignol S., Giroux N., Chau C., Marcoux J., Brustein E., Reader T.A. Pharmacological aids to locomotor learning after spinal cord injury in the cat. J. Physiol. (Lond.). 533:2001;65-74.
121. Sayer F.T., Oudega M., Hagg T. Neurotrophins reduce degeneration of injured ascending sensory axons and corticospinal motor axons in adult rat spinal cord. Exp. Neurol. 175:2002;282-296.
122. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell. 103:2000;211-225.
123. Schwab M.E. Inhibition of axonal growth by the myelin-associated inhibitory proteins NI-35/250/Nogo-a. Ingoglia N.A., Murray M. Axonal Regeneration in the Central Nervous System. 2001;411-423 Marcel Dekker, Inc, New York, NY.
124. Seddon H. Surgical Disorders of the Peripheral Nerve. 1972;1-332 Williams and Wilkins, Baltimore.
125. Shibata, M., Murray, M., Tessler, A., Ljubetic, C., Saavedra, R.A., 2000. Single injections of a DNA plasmid that contains human bcl-2 gene prevent loss and atrophy of distinct neuronal populations after spinal cord injury in adult rats. Neurorehabilitation Neural Repair 14, 319-330.
126. Shuman S.L., Bresnahan J.C., Beattie M.S. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J. Neurosci. Res. 50:1997;798-808.
127. Stokes B.T., Reier P.J. Fetal grafts alter chronic behavioural outcome after contusion damage to the adult rat spinal cord. Exp. Neurol. 116:1992;1-12.
128. Storer, P.D., Houle, J.D., 2002. Changes in βII-tubulin and GAP 43 mRNA expression in chronically injured neurons following a second spinal cord injury. Soc. Neurosci. Abstr. 824.6.
129. Strittmatter S.M. Modulation of axonal regeneration in neurodegenerative disease focus on Nogo . J. Mol. Neurosci. 19:2002;117-121.
130. Sulaiman O.A., Gordon T. Effects of short-and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia. 32:2000;234-246.
131. Sunderland S. Nerve Injuries and Their Repair. 1991;1-538 Churchill Livingstone, Edinburgh.
132. Takahashi K., Schwartz E., Ljubetic C., Murray M., Tessler A., Saavedra R. A DNA plasmid that codes for the human BC12 gene preserves axotomized Clarke's nucleus neurons and reduces atrophy after spinal hemisection in adult rats. J. Comp. Neurol. 404:1999;159-171.
133. Tang S., Woodhall R.W., Shen Y.J., deBallard M.E., Saffell J.L., Doherty P., Walsh F.S., Filbin M.T. Soluble myelin-associated glycoprotein (MAG) found in vivo inhibits axonal regeneration. Mol. Cell Neurosci. 9:1997;333-346.
134. Teng Y.D., Lavik E.B., Qu X., Park K.I., Ourednik J., Zurakowski D., Langer R., Snyder E.Y. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl. Acad. Sci. USA. 99:2002;3024-3029.
135. Thallmair M., Metz G.A.S., Z'Graggen W.J., Raineteau O., Kartje G.L., Schwab M.E. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci. 1:1998;124-131.
136. Thanos S., Vanselow J. Adult retinal ganglion cells retain the ability to regenerate their axons up to several weeks after axotomy. J. Neurosci. Res. 22:1989;144-149.
137. Tillakaratne N.J.K., de Leon R.D., Hoang T.X., Roy R.R., Edgerton V.R., Tobin A.J. Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J. Neurosci. 22:2002;3130-3143.
138. Tobias, C.A., Shibata, M., Shumansky, J.S., Tumulo, M., Tuszynski, M.H., Fischer, I., Tessler, A., Murray, M., 2001. Grafting of BDNF and NT-2 producing fibroblasts into the chronically injured adult rat cervical spinal cord. Soc. Neurosci. Abstr. 369.8.
139. Tseng G.-F., Shu J., Huang S.-J., Wang Y.-J. A time-dependent loss of retrograde transport ability in distally axotomized rubrospinal neurons. Anat. Embryol. 191:1995;243-249.
140. Vidal-Sanz M., Bray G.M., Villegas-Perez M.P., Thanos S., Aguayo A.J. Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in adult rats. J. Neurosci. 7:1987;2894-2909.
141. von Mayenburg J., Brösamle C., Metz G.A.S., Schwab M.E. Regeneration and sprouting of chronically injured corticospinal tract fibers in adult rats promoted by NT-3 and the mAb IN-1, which neutralizes myelin-associated neurite growth inhibitors. Exp. Neurol. 154:1998;583-594.
142. Wang X., Chun S.J., Treloar H., Vartanian T., Greer C.A., Strittmatter S.M. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 22:2002;5505-5515.
143. Weidner N., Grill R.J., Tuszynski M.H. Elimination of basal lamina and the collagen "scar" after spinal cord injury fails to augment corticospinal tract regeneration. Exp. Neurol. 160:1999;40-50.
144. Wernig A., Muller S., Nanasy A., Cagol E. Laufband therapy based on "rules of spinal Locomotion" is effective in spinal cord injured persons. Eur. J. Neurosci. 7:1999;823-829.
145. Wizenmann A., Thies E., Klostermann S., Bonhoeffer F., Bahr M. Appearance of target-specific guidance information for regenerating axons after CNS lesions. Neuron. 11:1993;975-983.
146. Woerly S., Doan V.D., Evans-Martin F., Paramore C.G., Peduzzi J.D. Spinal cord reconstruction using Neurogel™ implants and functional recovery after chronic injury. J. Neurosci. Res. 66:2001;1187-1197.
147. Wolpaw J.R., Tennisen A.M. Activity-dependent spinal cord plasticity in health and disease. Annu. Rev. Neurosci. 24:2001;807-843.
148. Xu X.M., Guenard V., Kleitman N., Aebischer P., Bunge M.B. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in the adult rat spinal cord. Exp. Neurol. 134:1995;261-272.
149. Yakoleff A., Cabelguen J.M., Orsal D., Giménez y Ribotta M., Rajaofetra N., Drian M.J., Bussel B., Privat A. Fictive motor activities in adult chronic spinal rats transplanted with embryonic brainstem neurons. Exp. Brain Res. 106:1995;69-78.
150. Ye J.H., Houle J.D. Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143:1997;70-81.