Spinal cord repair strategies: Schwann cells, neurotrophic factors, and biodegradable polymers

Biomedical Reviews

Volumn 10, Issue 1, 1999, Pages 75-88

  Oudega, Martin ^a,b   Gautier, Sandrine E ^a,b  

^a UNIVERSITY OF MIAMI   (United States)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0347374934     PISSN: 1310392X     EISSN: None     Source Type: Journal    
DOI: 10.14748/bmr.v10.10     Document Type: Article

References (142)

1. Abe Y, Yamamoto T, Sugiyama Y, Watanabe T, Saito N, Kayama H et al. Apoptotic cell cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendrocyte death. J Neurotrauma 1999;16:945-952.
2. Aguayo AJ. Capacity for renewed axonal growth in the mammalian central nervous system. In: Bignami A, Bloom FE, Bolis CL, Adeloye A, editors. Central Nervous System Plasticity and Repair. Raven Press, New York. 1958; pp: 31-40.
3. ALS-CNTF-Treatment-Study-Group. A double-blind placebo-controlled clinical trial of subcutaneous recombinant human ciliary neurotrophic factor (rHCNTF) in amyotrophic lateral sclerosis. Neurology 1996; 46:1244-1249.
4. Anderson DK, Howland DR, Reier PJ. Fetal neural grafts and repair of the injured spinal cord. Brain Pathol 1995; 5:451-457.
5. Atala A, Freeman MR, Vacanti JP, Shepard J, Retik AB Implantation in vivo and retrival of artificial structures consisting of rabbit and human urothelium and human bladder muscle. J Urol 1993; 150:608-612.
6. Athanasiou KA, Nicderauer GG, Agrawal CM. Sterilization, toxicity, biocompatibility and clinical applications of polylactic/polyglycolicacid copolymers Biomaterials 1996; 17:93-102.
7. Barbacid M. Neurotrophic factors and their receptors. Curr Opin Cell Biol 1995; 7:148-155.
8. Barrcs BA. Raff MC, Gaese F, Bartke I, Dechant G, Barde YA. A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 1994;367:371-375.
9. Bartholdi D, Schwab ME. Methylprednisolone inhibitsearly inflammatory processes but not ischemic cell death after experimental spinal cord lesion in the rat. Brain Res 1995; 672:177-186.
10. Benoit J-P, Menei P, Boisdron M, Gamelin E, Guy G. Radiosensitization of glioblastoma after intracranial implantaion of biodegradable 5-FU-Ioaded microspheres: Phase I/II clinical trial, [abstarct]. Proc Int Symp Control Rel Bioact Mater 1997; 24:995.
11. Beumer G, van Blitterswik CA, Ponec M. Biocompatibility of a biodegradable matrix used as a skin substitute: An in vivo evaluation. J Biomed Mater Res 1994; 28:545-552.
12. Blesch A, Tuszynski MH. Robust growth of chronically injured spinal cord axons induced by grafts of genetically modified NGF-secrcting cells. Exp Neurol 1997; 148:444-453.
13. Blight AR. Delayed demyelination and macrophage invasion: a candidate for secondary cell damage in spinal cord injury. Cent Nerv Syst Trauma 1985;2:299-315.
14. Bisby MA, Tctzlaff W. Changes in cytoskelctal protein synthesis following axon injury and during axon regeneration. Mol Neurobiol 1992; 6:107-123.
15. Bothwell M. Functional interactions of neurotrophins and neurotrophin receptors. Annu Rev Neurosci 1995; 18:223-2153.
16. Bracken MB, Holford TR. Effects of timing of methylprednisolone or naloxone administration on recovery of segmental and long-tract neurological function in NASCIS 2. J Neurosurg 1993;79:500-507.
17. Bracken MB, Shepard MJ, Collins WF, Holford TR, Baskin DS, Eisenberg HM et al. Methylprednisolone or naloxone treatment after acute spinal cord injury: 1-Year follow-up data. J Neurosurg 1992;76:23-31.
18. Bracken MB, Shepard MJ, Holford TR, Leo-Summers L, Aldrich EF, Fazl M et al. Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. National Acute Spinal Cord Injury Study. JAMA 1997; 277:1597-1604.
19. ; Gao D, Schwab ME. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 1995; 378: 498-501.
20. Bregman BS, Diener PS, McAtee M, Dai HN, James C. Intervention strategies to enhance anatomical plasticity and recovery of function after spinal cord injury. Adv Neurol 1997;72:257-275.
21. Bregman BS. Broude E, McAtee M. Kelley MS. Transplants and neurotrophic factors prevent atrophy of mature CNS neurons afterspinal cord injury. Exp Neurol 1998; 149:13-27.
22. Bunge RP. Expanding roles for the Schwann cell: ensheathment. myelination, trophism and regeneration. Curr Opin Neurobiol 1993; 3:805-809.
23. Bunge MB. Transplantation of purified populations of Schwann cells into lesioncd adult rat spinal cord. J Neurol 1994;241:36-39.
24. Bunge MB, Kleitman N. Schwann cells as facilitators of axonal regeneration in CNS fiber tracts. In: Juurlink et al, editors. Cell Biology and Pathology of Myelin. Plenum Press, New York. 1997; pp:319-333.
25. Bunge RP, Puckett WR, Hiester ED. Observations on the pathology of several types of human spinal cord injury, with emphasis on the astrocytic response to penetrating injuries. Adv Neurol 1997; 72:305-315.
26. Bunge MB, Kleitman N. Ncurotrophins and neuroprotection improve axonal regeneration into Schwann cell transplants placed in transected adult rat spinal cord. In: CNS Regeneration. Academic Press, New York. 1998; pp 631-645.
27. Cadelli D, Schwab ME. Regeneration of Iesioned scpto-hippocampal acetylcholinesterase-positive axons is improved by antibodies against the myelin-associated neurite growth inhibitors NI-35/250. Eur J Neurosci 1991; 3:825-832
28. Campenot RB. NGF and the local control of nerve terminal growth. J Neurobiol 1995;20:599-611.
29. Casella GT, RP Bunge, PM Wood. Improved method for harvesting human Schwann cells from mature peripheral nerve and expansion in vitro. Glia 1996; 17:327-338.
30. Chao MV. Ceramidc: a potential second messenger in the nervous system. Mol Cell Neurosci 1995; 6:91-96.
31. Chao MV, Hempstead BL. p75 and Trk: a two-receptor system. Trends Neurosci 1995; 18:321-326.
32. Chen A, Xu XM, Kleitman N, Bunge MB. Methylprednisilone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp Neurol 1996; 138:261-276.
33. Cheng H, Olson L. A new surgical technique that allows proximodistal regeneration of 5-HT fibers after complete transection of the ratspinal cord. Exp Neurol 1995; 136:149-161.
34. Cheng H, Cao Y, Olson L. Spinal cord repair in adult paraplegic rats: Partial restoration of hind limb function. Science 1996;273:510-513.
35. David S, Aguayo AJ. Axonal elongation in peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 1981;214:931-933.
36. Davis MW. Vacanti JP. Toward development of an implantable tissue engineered liver. Biomaterials 1996; 17:365-372.
37. Davies SJA, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997; 390:680-683.
38. DeKosky ST, Styren SD, O'Malley ME, Goss JR, Kochanek P, Marion D et al. Interleukin-I receptor antagonist suppresses neurotrophin response in injured rat brain. Ann Neurol 1996;39:123-127.
39. Demopoulos HB, Flamm ES, Rietronigro DD, Seligman, M. L. The free radical pathology and the microcirculation in the major central nervous system disorders. Acta Physiol Scand 1980;492(Suppl. 111):91-119.
40. Den Dunnen WFA, vander Lei B, Schakcnraad JM, Blaauw EH, Stokroos I, Pennings AJ et al. Long-term evaluation of nerve regeneration in a biodegradable nerve guide. Micro-surgeiy 1993; 14:508-515.
41. DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM et al. The ncurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 1992; 8: 983-993.
42. Dobrowski RT, Werner MH, Castellino AM, Chao MV, Hannun YA. Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 1994; 265: 1596-1599.
43. Emery E, Aldana P, Bunge MB, Puckett W, Srinivasan A, Keane RW et al. Apoptosis after traumatic human spinal cord injury. J Neitrosurg 1998; 89:911-920.
44. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999; 49:377-91.
45. Field RD, Lc Beau JM, Longo FM, Ellisman MH. Nerve regeneration through artificial tubular implants. Prog Neurobiol 1989;33:87-134.
46. Frade JM, Rodriguez-Tebar A, Bardc YA. Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 1996;383:166-168.
47. Gautier SE, Oudega M, Fragoso M, Chapon P, Plant GW, Bunge MB et al. Poly(α-hydroxyacids for application in the spinal cord: Resorbability and biocompatibility with adult rat Schwann cells and spinal cord. J Biomed Mater Res 1998; 42:642-654.
48. Gilson BC, Stcnsaas LJ. Early axonal changes following lesions of the dorsal columns in rats. Cell Tiss Res 1974149: 1-20.
49. Giovanini MA, Reier PJ, Eskin TA, Wirth E, Anderson DK. Characteristics of human fetal spinal cord grafts in the adult rat spinal cord: influences of lesion and grafting conditions. Exp Neurol 1997; 148:523-543.
50. Giulian D, Robertson C. Inhibition of mononuclear phagocytes reduces ischemic injury in thespinal cord. Ann Neurol 1990;27:33-42.
51. Grafstein B, McQuarrie IG. Role of the nerve cell body in axonal regeneration. In: Cotman CW, editor. Neuronal Plasticity. Raven Press, New York. 1978; pp 155-195.
52. Granholm AC, Backman C, Bloom F, Ebendal T, Gerhardt GA, Hoffer B et al. NGF and anti-transferrin receptor antibody conjugate: short and long-term effects on survival of cholinergic neurons in intraocular septal transplants. J Pharmacol Exp Ther 1994; 268:448-459.
53. Grill R, Murai K. Blcsch A, Gage FH, Tuszynski MH. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 1997; 17:5560-5572.
54. Guènard V, Xu XM, Bunge MB. The use of Schwann cell transplantation to foster central nervous system repair. Sent Neurosä 1993;5:401-411.
55. Guest JD, Rao A, Olson L, Bung e MB, Bunge RP. The ability of human Schwann cell grafts to promote regeneration in the transected nuderatspinal cord. Exp Neurol 1997; 148:502-522.
56. Gundersen RW, Barrett JN. Characterization of the turning response of dorsal root neurites toward nerve growth factor. J Cell Biol 1980; 87:546-554.
57. Hagg T, Vahlsing HL, Manthorpe M. Varon S. Nerve growth factor infusion into the denervated adult rat hippocampal formation promotes its cholinergic reinnervation. J Neurosci 1990;10:3087-3092.
58. Heumann R. Neurotrophinsignalling. Ciirr Opin Neurobiol 1994;4:668-679.
59. Hoffman D, Wahlberg L, Aebischer P. NGF released from a polymer matrix prevents loss of ChAT expression in basal forcbrain neurons following a fimbria-fornix lesion. Exp Neurol 1990; 110:39-44.
60. Horner PJ, Reier PJ, Stokes BT. Quantitative analysis of vascularization and cytochrome oxidase following fetal transplantation in the contused rat spinal cord. J Conip Neurol 1996;364:690-703.
61. Houle JD. Regeneration of dorsal root axons is related to specific non-neuronal cells lining NGF-treated intraspinal nitrocellulose implants. Exp Neurol 1992; 118:133-142.
62. Ibanez CF. Neurotrophic factors: from structure-function studies to designing effective therapeutics. Trends Bioteclmol 1995; 13:217-227.
63. Johanson SO, Crouch MF, Hendry IA. Signal transduction from membrane to nucleus: the special case for neurons. Neurochem Res 1996;21:779-785.
64. Joosten EAJ, Bar PR, Gispen WH. Collagen implant and corticospinal axonal growth after mid-thoracic spinal cord lesion in adult rat. J Neurosci Res 1995;41:481-490.
65. Kao CC, Chang LW, Bloodvvorth JMB. The mechanism of spinal cord cavitation following spinal cord transaction. J Neurosurg 1977;46:197-209.
66. Khan T, Dauzvardis M, Sayers S. Carbon filament implants promote axonal growth across the transected rat spinal cord. Brain Res 1991;541:139-145.
67. Kim DH, Gutin PH, Noble LJ, Nathan D, Yu JS, Nockcls RP. Treatment with genetically engineered fibroblasts producing NGF or BDNF can accelerate recovery from traumatic spinal cord injury in theadult rat. Neuro Report 1996; 7:2221-2225.
68. Kordowcr JH, Charles V, Bayer R, Bartus RT, Putney S, Walus LR et al. Intravenous administration of a transferrin receptor antibody-nerve growth factor conjugate prevents the degeneration of cholinergic striatal neurons in a model of Huntington disease. Proc Natl Acad Sci USA 1994; 91: 9077-9080.
69. Kou JH, Emmett C, Shen P, Aswani S, Iwamoto T, Vaghefi F et al. Bioerosion and biocompatibility of poly(D, L-lactic-co-glycolic acid) implants in the brain. J Control Rel 1997; 43: 123-130.
70. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996; 19:312-318.
71. Levi AD, Bunge RP, Lofgren JA, Meina L, Hefti F, Nikolics K et al. The influence of heregulins on human Schwann cell prolifcration. J Neurosci 1995; 15:1329-1340.
72. Levi-Montalcini R. The nerve growth factor 35 years later. Science 1987;237:1154-1162.
73. Li Y, Field PM, Raisman G. Repairof adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 1997;277:2000-2003.
74. Lieberman AR. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol 1971;14:49-124.
75. Liu Y, Kim D, Himes BT, Chow SY, Schallert T, Murray M et al. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of rat rubrospinal axons and recovery of forelimb function. J Neurosci 1999; 19:4370-4387.
76. Louis JC, Magal E, Takayama S, Varon S. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 1993; 259:689-692.
77. MacKinnon SE, Lee Dellon A. Clinical nerve reconstruction with a bioabsorbable polygly colic acid tube. Plastic Reconstr Surg 1988;85:419-423.
78. Maquet V, Jérôme R. Design of macroporous biodegradable polymer scaffold for cell transplantation. In: Porous Materials for Tissue Engineering. Trans Tech Publications, Utikon-Zurich. 1997; pp 15-42.
79. Maquet V, Martin D, Malgrange B, Franzen R, Schoenen J, Moonen G et al. Peripheral nerve regeneration using bioresorbable macroporous polylactide scaffolds. J Biomed Mater Res (Submitted).
80. Maquet V, Martin D, Schoenen J, Moonen G, Jérôme R. Poly(D, L-Iactide) foams modified with poly(ethy Ienc oxide)-block-poly(D, L-lactide)copolymers: in vitro degradation and in vivo implantation for axonal regeneration in the injured spinal cord. J Biomat Sci (Submitted).
81. Marchand R, Woerly S, Bertrand L, Valdes N. Evaluation of two cross-linked collagen gels implanted in the transected spinal cord. Brain Res Bull 1993; 30:415-422.
82. Martin D, Robe P, Franzen R, Delree P, Schoenen J, Stevenaert A et al. Effects of Schwann cell transplantation in a contusion model of rat spinal cord injury. J Neurosci Res 1996; 45: 588-597.
83. McCormack M, Goddard M, Guénard V, Aebisher P. Comparison of dorsal and ventral spinal root regeneration through semipermeable guidance channels. J Comp Neurol 1991; 313:449-456.
84. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE. Identification of myclin-associated glycoprotein as amajormyelin-derived inhibitor of neuritc growth. Neu-ron 1994; 13:805-811.
85. McTiguc DM, Horner PJ, Stokes BT, Gage FH. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 1998; 15: 5354-5365.
86. Menei P, Daniel V, Montero-Menei C, Brouillard M, Pouplart-Barthelaix A, Benoit J-P. Biodegradation and brain tissue reaction to poly(D, L-lactide-co-glycolide) microspheres. Biomaterials 1993; 14:470-478.
87. Menei P, Benoit JP, Boisdron-Celle M, Fournier D, Mercier P, Guy G. Drug targeting into the central nervous system by stereotactic implantation of biodegradable microspheres. Neurosurgery 1994; 34:1058-1064.
88. Menei P, Montero-Menei C, Whittemore SR, Bunge RP, Bunge MB. Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. Eur J Neurosci 1998; 10:607-621.
89. Mocchetti I, Wrathall JR. Neurotrophic factors in central nervous system trauma. JNeurotrauma 1995; 12:853-870.
90. Morrissey TK, Kleitman N, Bunge RP. Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J Neurosci 1991; 11:2433-2442.
91. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT. A novel role for myelin-associatcd glycoprotein as an inhibitor of axonal regeneration. Neuron 1994; 13:757-767.
92. Oppenheim RW. The concept of uptake and retrograde transport of neurotrophic molecules during development: history and present status. Neurochem Res 1996; 21:769-777.
93. Oudega M, Varon S, Hagg T. Regeneration of adult rat sensory axons into intraspinal nerve grafts: promoting effects of conditioning lesion and graft predegencration. Exp Neurol 1994:129:194-206.
94. Oudega M, Hagg T. Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp Neurol 1996; 140:218-229.
95. Oudega M, Hagg T. Neurotrophic promote regeneration of sensory axons in the adult rat spinal cord. Brain Res 1999;818:431-438.
96. Oudega M, Xu XM. Guenard V, Kleitman N. Bunge MB. A combination of insulin-like growth factor and platelet-derived growth factor enhances myelination but diminishes axonal regeneration into Schwann cell grafts in the adult rat spinal cord. Glia 1997; 19:247-258.
97. Oudega M, Gautier SE, Fragoso M, Plant GW. Bungc MB, Parel J-M. In vitro and in vivo studies on bioresorbable poly (α-hydroxyacids) constructs for the application of Schwann cells in spinal cord regeneration. Soc Biomat 1998; 349.
98. Oudega M Vargas CG, Weber AB, Kleitman N, Bunge MB. Long-term effects of methylprednisolone following transec-tionof adult rat spinal cord. Eur J Neurosci 1999; 11:2453-2464.
99. Oudega M, Plant GW, Katz J, Marcillo A, Bunge MB. Schwann cell and ensheathing glia transplantation into the contusion injured adult rat spinal cord. Soc Neurosci Abstr 1999;25:295.
100. Pasterkamp RJ, De Winter F, Giger RJ, Verhaagen J. Role of semaphorin III and its receptor neuropilin-1 in neuronal regeneration and scar formation? Prog Brain Res 1998; 117:151-170.
101. Pindzola RR, Doller C, Silver J. Putativeinhibitory extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesions. Dev Biol 1993;156:34-48.
102. Pollock M. Nerve regeneration. Curr Opin Neurol 1995; 8:354-358.
103. Rabizadch S, Oh J, Zhong LT, Yang J, Bidcr CM, Butcher LL et al. Induction of apoptosis by the low-affinity NGF receptor. Science 1993; 261:345-348.
104. Ramon-Cueto A, Nicto-Sampedro M. Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp Neurol 1994; 127: 232-244.
105. Ramon-Cueto A, Plant GW, Avila J, Bunge MB. Longdistance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci 1998; 18:3803-3815.
106. Ramon-Cucto A, Cordero MI, Santos-Benito FF, Avila J. Olfactory ensheathing glia transplants promote functional recovery and structural repair of transected adult rat spinal cords. Soc Neurosci Abstr 1999; 25:295.
107. Ramony Cajal S. Degeneration and Regeneration of the Nervous System. May RM, translator. Oxford University Press, London. 1928.
108. Reid RL, Cutright DE, Garrison JS. Biodegradable cuff an adjunct to peripheral nerve repair: A study in dogs. Hand 1978;10:259-266.
109. Reier PJ, Anderson DK, Thompson FJ, Stokes BT. Neural tissue transplantation and CNS trauma: anatomical and functional repair of the injured spinal cord. J Neurotrauma 1992;9:S223-248.
110. Reier PJ, Stokes BT, Thompson FJ, Anderson DK. Fetal cell grafts into resection and contusion/compression injuries oftheratandcatspinalcord. Exp Neurol 1992;115:177-188.
111. Richardson PM. Neurotrophic factors in regeneration. Curr Opin Neurobiol 1991; 1:401-406.
112. Richardson PM McGuinness UM, Aguayo AJ. Axons from CNS neurons regenerate into PNS grafts. Nature 1980;284:264-265.
113. Rosenberg MB, Friedmann T, Robertson RC, Tuszynski M, Wolff JA, Breakefield XO et al. Grafting genetically modified cells to the damaged brain: restorative effects of NGF expression. Science 1988;242:1575-1578.
114. Rutkowski JL. Kirk CJ. Lerner MA. Tennekoon GI. Purification and expansion of human Schwann cells in vitro. Nat Med 1995; 1:80-83.
115. Saporito MS, Brown ER, Hartpence KC, Wilcox HM, Robbins E, Vaught JL et al. Systemic dexamethasonc administration increases septal Trk autophosphorylation in adult rats via an induction of nerve growth factor. Mol Pharmacol 1994;45:395-401.
116. Sayer F, Oudega M, Hagg T. Neurotrophins prevent degeneration of proximal stumps of transacted sensory axons in adult rat spinal cord. Soc Neurosci Abstr 1996; 745.
117. Schnell L, Schneider R. Kolbeck R. Barde YA. Schwab ME. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 1994;367:170-173.
118. Schnell L, Schwab ME. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neuritc growth inhibitors. Nature 1990; 343: 269-272.
119. Schnell L, Schwab ME. Sprouting and regeneration of Icsioned corticospinal tract fibers in the adult rat spinal cord. Eur J Neurosci 1993;5:1156-1171.
120. Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lcsioned spinal cord. Physiol Rev 1996;76: 319-370.
121. Schwab ME. Kapfhammer JP. Bandflow CE. Inhibitors of neurite growth. Ann Rev Neurosci 1993; 16:565-595.
122. Segal RA. Greenberg ME. Intracellular signaling pathways activated by neurotrophic factors. Ann Rev Neurosci 1996; 19:463-489.
123. Senut MC, Tusynski MH, Raymon HK, Suhr ST, Liou NH, Jones KR et al. Regional differences in responsiveness of adult CNS axons to grafts of cells expressing human neurotroρhin3. Exp Neurol 1995; 135:36-55.
124. Spranger M, Lindholm D, Bandtlow C, Heumann R, Gnahn H, Naher-Noe M et al. Regulation of nerve growth factor (NGF) synthesis in the central nervous system: comparison between the effects of ǐnterleukin-1 and various growth factors in astrocyte cultures and in vivo. Eur J Neurosci 1990; 2:69-76.
125. Tator CH, Fehlings MG. Review of the secondary injury theory of spinal cord trauma with emphasis on vascular mechanisms. J Neurosurgery 1991; 75:15-26.
126. Tessler A. Intraspinal transplants. Ann Neurol 1991; 29: 115-123.
127. Tetzlaff W, Alexander SW, Miller FD, Bisby MA. Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins abd GAP-43. J Neurosci 1991; 11:2528-2544.
128. Tetzlaff W, Kobayashi NR, Giehl KMG. Tsui BJ. Cassar SL, Bedard AM. Response of rubrospinal and corticospinal neurons to injury and neurotrophins. Prog Brain Res 1994; 103:271-286.
129. Tuszynski MH, Peterson DA, Ray J, Baird A, Nakahara Y, Gage FH. Fibroblasts genetically modified to produce nerve growth factor induce robust neuritic ingrowth after grafting to the spinal cord. Exp Neurol 1994; 126: 1-14.
130. Tuszynski MH. Weidner N. McCormack M, Miller I, Powell H, Conner J. Grafts of genetically modified Schwann cells to the spinal cord: survival, axon growth, and myelination. Cell Transplant 1998; 7:187-196.
131. Tuszynski MH, Gabriel K, Gerhardt K, Szollar S. Human spinal cord retains substantial structural mass in chronic stages after injury. J Neurotrauma 1999; 16:523-531.
132. Vert M, Li SM, Garreau H. Attempts to map the structure and degradation characteristics of aliphatic polyesters derived from lactic and glycolic acids. Biomater Sci Polym. 1994;6:639-649.
133. Weibel D, Kreutzberg GW, Schwab ME. Brain-derived neurotrophic factor (BDNF) prevents lesion-induced axonal die-back in young rat optic nerve. Brain Res 1995; 679: 249-254.
134. Weidner N, Blesch A, Grill RJ, Tuszynski MH. Nerve growth factor-hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and myelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1. J Comp Neurol 1999;413:495-506.
135. Woerly S, Pinet E, De Robertis L, Bousmina M, Laroche G, Roitback T et al. Heterogeneous PHPMA hydrogels for tissue repair and axonal regeneration in the injured spinal cord. J Biomater Sci Polymer 1998; 9:681-711.
136. Wrathall JR, Rigamonti DD, Bradford MR, Kao CC. Reconstruction of the contused cat spinal cord by the delayed nerve graft technique and cultured peripheral non-neu-ronal cells. Acta Neuropathol 1982; 57:59-69.
137. Xu XM, Guénard V, Kleitman N, Bunge MB. Axonal regeneration into Schwann cell seeded guidance channels-grafted into transected adult rat spinal cord. J Comp Neurol 1995; 351:145-160.
138. Xu XM, Guénard V, Kleitman N, Aebischer P, Bunge MB. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp Neurol 1995; 134:261-272.
139. Xu XM, Chen A, Guénard V, Kleitman N, Bunge MB. Bridging Schwann cell transplants promote axonal regeneration from both the proximal and distal stumps of transacted adult rat spinal cord. J Neiirocytol 1997;26: 1-16.
140. Xu XM, Bamber NI, Li H, Lu X, Aebischer P, Oudega M. Axonal regrowth and reentry into the distal spinal cord of adult rats following transplantation of Schwann cell seeded mini-channels and infusion of two neurotrophins, BDNF and NT-3, into the distal spinal cord. Exp Neurol 1998; 151:158.
141. Zhang Z, Krebs CJ, Guth L. Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp Neurol 1997;143:141-152.
142. Zuo J, Neubauer D, Dyess K, Ferguson TA, Muir D. Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp Neurol 1998; 154:654-662.