Neurotrophic factors for spinal cord repair: Which, where, how and when to apply, and for what period of time?

Brain Research

Volumn 1619, Issue , 2015, Pages 36-71

  Harvey, Alan R ^a   Lovett, Sarah J ^a   Majda, Bernadette T ^a   Yoon, Jun H ^a   Wheeler, Lachlan P G ^a   Hodgetts, Stuart I ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Brain derived neurotrophic factor; Cell death; Ciliary neurotrophic factor; Fibroblast growth factor; Glial cell derived neurotrophic factor; Nerve growth factor; Neurotrophic factors; Neurotrophin 3; Plasticity; Platelet derived neurotrophic factor; Regeneration; Spinal cord injury

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; POLYMER; RECOMBINANT PROTEIN; NERVE GROWTH FACTOR;

ARTICLE; CELL BODY; CELL DEATH; CELL SURVIVAL; DRUG RELEASE; GLIA CELL; HUMAN; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER; NERVE SPROUTING; NERVE TRANSECTION; NEUROPROTECTION; NONHUMAN; NONVIRAL GENE THERAPY; OPTIC NERVE; OSMOTIC MINIPUMP; PRIORITY JOURNAL; RETINA GANGLION CELL; SPINAL CORD INJURY; SPINAL CORD REGENERATION; STEM CELL; SYNAPTOGENESIS; TISSUE GRAFT; ANIMAL; DISEASE MODEL; DRUG EFFECTS; METABOLISM; NERVE CRUSH; SPINAL CORD; SPINAL CORD INJURIES;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; NERVE CRUSH; NERVE GROWTH FACTORS; SPINAL CORD; SPINAL CORD INJURIES; SPINAL CORD REGENERATION;

EID: 84962259323     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.10.049     Document Type: Article

References (220)

1. A. Abdanipour, T. Tiraihi, and T. Taheri Intraspinal transplantation of motoneuron-like cell combined with delivery of polymer-based glial cell line-derived neurotrophic factor for repair of spinal cord contusion injury Neural Regen. Res. 9 2014 1003 1013
2. L.T. Alto, L.A. Havton, J.M. Conner, E.R. Hollis 2nd, A. Blesch, and M.H. Tuszynski Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury Nat. Neurosci. 12 2009 1106 1113
3. E. Ansorena, P. De Berdt, B. Ucakar, T. Simon-Yarza, D. Jacobs, O. Schakman, A. Jankovski, R. Deumens, M.J. Blanco-Prieto, V. Preat, and A. des Rieux Injectable alginate hydrogel loaded with gdnf promotes functional recovery in a hemisection model of spinal cord injury Int. J. Pharm. 455 2013 148 158
4. V. Arvanian Role of neurotrophins in spinal plasticity and locomotion Curr. Pharm. Des. 19 2013 4509 4516
5. B.I. Awad, M.A. Carmody, and M.P. Steinmetz Potential role of growth factors in the management of spinal cord injury World Neurosurg 2013
6. K.A. Baker, S. Nakashima, and T. Hagg Dorsal column sensory axons lack trkc and are not rescued by local neurotrophin-3 infusions following spinal cord contusion in adult rats Exp. Neurol. 205 2007 82 91
7. N.I. Bamber, H. Li, X. Lu, M. Oudega, P. Aebischer, and X.M. Xu 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 2001 257 268
8. D.M. Basso, L.C. Fisher, A.J. Anderson, L.B. Jakeman, D.M. McTigue, and P.G. Popovich Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains J. Neurotrauma 23 2006 635 659
9. L. Benowitz, and Y. Yin Rewiring the injured CNS: lessons from the optic nerve Exp. Neurol. 209 2008 389 398
10. L.I. Benowitz, and P.G. Popovich Inflammation and axon regeneration Curr. Opin. Neurol. 24 2011 577 583
11. M. Berry, Z. Ahmed, B. Lorber, M. Douglas, and A. Logan Regeneration of axons in the visual system Restor. Neurol. Neurosci. 26 2008 147 174
12. A. Blesch, H.S. Uy, R.J. Grill, J.G. Cheng, P.H. Patterson, and M.H. Tuszynski Leukemia inhibitory factor augments neurotrophin expression and corticospinal axon growth after adult CNS injury J. Neurosci. 19 1999 3556 3566
13. A. Blesch, and M.H. Tuszynski Cellular GDNF delivery promotes growth of motor and dorsal column sensory axons after partial and complete spinal cord transections and induces remyelination J. Comp. Neurol. 467 2003 403 417
14. A. Blesch, H. Yang, N. Weidner, A. Hoang, and D. Otero Axonal responses to cellularly delivered NT-4/5 after spinal cord injury Mol. Cell. Neurosci. 27 2004 190 201
15. A. Blesch, and M.H. Tuszynski Transient growth factor delivery sustains regenerated axons after spinal cord injury J. Neurosci. 27 2007 10535 10545
16. A. Blesch, I. Fischer, and M.H. Tuszynski Gene therapy, neurotrophic factors and spinal cord regeneration Handb. Clin. Neurol. 109 2012 563 574
17. B. Blits, M. Oudega, G.J. Boer, M. Bartlett Bunge, and J. Verhaagen Adeno-associated viral vector-mediated neurotrophin gene transfer in the injured adult rat spinal cord improves hind-limb function Neuroscience 118 2003 271 281
18. V.S. Boyce, M. Tumolo, I. Fischer, M. Murray, and M.A. Lemay Neurotrophic factors promote and enhance locomotor recovery in untrained spinalized cats J. Neurophysiol. 98 2007 1988 1996
19. V.S. Boyce, J. Park, F.H. Gage, and L.M. Mendell Differential effects of brain-derived neurotrophic factor and neurotrophin-3 on hindlimb function in paraplegic rats Eur. J. Neurosci. 35 2012 221 232
20. V.S. Boyce, and L.M. Mendell Neurotrophins and spinal circuit function Front. Neural Circuits 8 2014 59
21. E.J. Bradbury, V.R. King, L.J. Simmons, J.V. Priestley, and S.B. McMahon NT-3, but not BDNF, prevents atrophy and death of axotomized spinal cord projection neurons Eur. J. Neurosci. 10 1998 3058 3068
22. E.J. Bradbury, S. Khemani, R. Von, King, J.V. Priestley, and S.B. McMahon NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur. J. Neurosci. 11 1999 3873 3883
23. B.S. Bregman, M. McAtee, H.N. Dai, and P.L. Kuhn Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat Exp. Neurol. 148 1997 475 494
24. B.S. Bregman, J.V. Coumans, H.N. Dai, P.L. Kuhn, J. Lynskey, M. McAtee, and F. Sandhu Transplants and neurotrophic factors increase regeneration and recovery of function after spinal cord injury Prog. Brain Res. 137 2002 257 273
25. J.H. Brock, E.S. Rosenzweig, A. Blesch, R. Moseanko, L.A. Havton, V.R. Edgerton, and M.H. Tuszynski Local and remote growth factor effects after primate spinal cord injury J. Neurosci. 30 2010 9728 9737
26. L. Cao, L. Liu, Z.Y. Chen, L.M. Wang, J.L. Ye, H.Y. Qiu, C.L. Lu, and C. He Olfactory ensheathing cells genetically modified to secrete gdnf to promote spinal cord repair Brain 127 2004 535 549
27. Q. Cao, X.M. Xu, W.H. Devries, G.U. Enzmann, P. Ping, P. Tsoulfas, P.M. Wood, M.B. Bunge, and S.R. Whittemore Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells J. Neurosci. 25 2005 6947 6957
28. Q. Cao, Q. He, Y. Wang, X. Cheng, R.M. Howard, Y. Zhang, W.H. DeVries, C.B. Shields, D.S. Magnuson, X.M. Xu, D.H. Kim, and S.R. Whittemore Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury J. Neurosci. 30 2010 2989 3001
29. L.P. Cen, J.M. Luo, C.W. Zhang, Y.M. Fan, Y. Song, K.F. So, N. van Rooijen, C.P. Pang, D.S. Lam, and Q. Cui Chemotactic effect of ciliary neurotrophic factor on macrophages in retinal ganglion cell survival and axonal regeneration Invest. Ophthalmol. Vis. Sci. 48 2007 4257 4266
30. F. Chehrehasa, M. Cobcroft, Y.W. Young, A. Mackay-Sim, and B. Goss An acute growth factor treatment that preserves function after spinal cord contusion injury J. Neurotrauma 31 2014 1 7
31. Q. Chen, L. Zhou, and H.D. Shine Expression of neurotrophin-3 promotes axonal plasticity in the acute but not chronic injured spinal cord J. Neurotrauma 23 2006 1254 1260
32. D. Cizkova, F. Le Marrec-Croq, J. Franck, L. Slovinska, I. Grulova, S. Devaux, C. Lefebvre, I. Fournier, and M. Salzet Alterations of protein composition along the rostro-caudal axis after spinal cord injury: proteomic, in vitro and in vivo analyses Front. Cell. Neurosci. 8 2014 105
33. M.P. Cote, G.A. Azzam, M.A. Lemay, V. Zhukareva, and J.D. Houle Activity-dependent increase in neurotrophic factors is associated with an enhanced modulation of spinal reflexes after spinal cord injury J. Neurotrauma 28 2011 299 309
34. J.V. Coumans, T.T. Lin, H.N. Dai, L. MacArthur, M. McAtee, C. Nash, and B.S. Bregman 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
35. Q. Cui, S.I. Hodgetts, Y. Hu, J.M. Luo, and A.R. Harvey Strain-specific differences in the effects of cyclosporin A and FK506 on the survival and regeneration of axotomized retinal ganglion cells in adult rats Neuroscience 146 2007 986 999
36. S.M. Dale, R.Z. Kuang, X. Wei, and S. Varon Corticospinal motor neurons in the adult rat: degeneration after intracortical axotomy and protection by ciliary neurotrophic factor (CNTF) Exp. Neurol. 135 1995 67 73
37. S. de Lima, Y. Koriyama, T. Kurimoto, J.T. Oliveira, Y. Yin, Y. Li, H.Y. Gilbert, M. Fagiolini, A.M. Martinez, and L. Benowitz Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors Proc. Natl. Acad. Sci. USA 109 2012 9149 9154
38. L.X. Deng, J. Hu, N. Liu, X. Wang, G.M. Smith, X. Wen, and X.M. Xu GDNF modifies reactive astrogliosis allowing robust axonal regeneration through Schwann cell-seeded guidance channels after spinal cord injury Exp. Neurol. 229 2011 238 250
39. L.X. Deng, P. Deng, Y. Ruan, Z.C. Xu, N.K. Liu, X. Wen, G.M. Smith, and X.M. Xu A novel growth-promoting pathway formed by GDNF-overexpressing Schwann cells promotes propriospinal axonal regeneration, synapse formation, and partial recovery of function after spinal cord injury J. Neurosci. 33 2013 5655 5667
40. M.R. Detloff, E.J. Smith, D. Quiros Molina, P.D. Ganzer, and J.D. Houle Acute exercise prevents the development of neuropathic pain and the sprouting of non-peptidergic (GDNF- and artemin-responsive) c-fibers after spinal cord injury Exp. Neurol. 255 2014 38 48
41. D. Dolbeare, and J.D. Houle Restriction of axonal retraction and promotion of axonal regeneration by chronically injured neurons after intraspinal treatment with glial cell line-derived neurotrophic factor (GDNF) J. Neurotrauma 20 2003 1251 1261
42. S.E. Dyson, A.R. Harvey, B.D. Trapp, and J.W. Heath Ultrastructural and immunohistochemical analysis of axonal regrowth and myelination in membranes which form over lesion sites in the rat visual system J. Neurocytol. 17 1988 797 808
43. M. Enomoto, M.B. Bunge, and P. Tsoulfas A multifunctional neurotrophin with reduced affinity to p75NTR enhances transplanted Schwann cell survival and axon growth after spinal cord injury Exp. Neurol. 248 2013 170 182
44. C. Fan, Y. Zheng, X. Cheng, X. Qi, P. Bu, X. Luo, D.H. Kim, and Q. Cao Transplantation of D15a-expressing glial-restricted-precursor-derived astrocytes improves anatomical and locomotor recovery after spinal cord injury Int. J. Biol. Sci. 9 2013 78 93
45. S.Q. Feng, X.H. Kong, Y. Liu, D.X. Ban, G.Z. Ning, J.T. Chen, S.F. Guo, and P. Wang Regeneration of spinal cord with cell and gene therapy Orthop. Surg. 1 2009 153 163
46. D. Fischer, and M. Leibinger Promoting optic nerve regeneration Prog. Retin. Eye Res. 31 2012 688 701
47. K. Fouad, L. Schnell, M.B. Bunge, M.E. Schwab, T. Liebscher, and D.D. Pearse Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord J. Neurosci. 25 2005 1169 1178
48. K. Fouad, and W. Tetzlaff Rehabilitative training and plasticity following spinal cord injury Exp. Neurol. 235 2012 91 99
49. K. Fouad, D.J. Bennett, R. Vavrek, and A. Blesch Long-term viral brain-derived neurotrophic factor delivery promotes spasticity in rats with a cervical spinal cord hemisection Front. Neurol. 4 2013 187
50. L. Frank, R. Ventimiglia, K. Anderson, R.M. Lindsay, and J.S. Rudge BDNF down-regulates neurotrophin responsiveness, Trkb protein and Trkb mrna levels in cultured rat hippocampal neurons Eur. J. Neurosci. 8 1996 1220 1230
51. T. Furuya, M. Hashimoto, M. Koda, A. Murata, A. Okawa, M. Dezawa, D. Matsuse, Y. Tabata, K. Takahashi, and M. Yamazaki Treatment with basic fibroblast growth factor-incorporated gelatin hydrogel does not exacerbate mechanical allodynia after spinal cord contusion injury in rats J. Spinal Cord Med. 36 2013 134 139
52. G. Garcia-Alias, H.A. Petrosyan, L. Schnell, P.J. Horner, W.J. Bowers, L.M. Mendell, J.W. Fawcett, and V.L. Arvanian Chondroitinase ABC combined with neurotrophin NT-3 secretion and NR2d expression promotes axonal plasticity and functional recovery in rats with lateral hemisection of the spinal cord J. Neurosci. 31 2011 17788 17799
53. C.G. Gerin, I.C. Madueke, T. Perkins, S. Hill, K. Smith, B. Haley, S.A. Allen, R.P. Garcia, T. Paunesku, and G. Woloschak Combination strategies for repair, plasticity, and regeneration using regulation of gene expression during the chronic phase after spinal cord injury Synapse 65 2011 1255 1281
54. K.L. Golden, D.D. Pearse, B. Blits, M.S. Garg, M. Oudega, P.M. Wood, and M.B. Bunge Transduced Schwann cells promote axon growth and myelination after spinal cord injury Exp. Neurol. 207 2007 203 217
55. Y. Goldshmit, T.E. Sztal, P.R. Jusuf, T.E. Hall, M. Nguyen-Chi, and P.D. Currie Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish J. Neurosci. 32 2012 7477 7492
56. Y. Goldshmit, F. Frisca, A.R. Pinto, A. Pebay, J.K. Tang, A.L. Siegel, J. Kaslin, and P.D. Currie Fgf2 improves functional recovery-decreasing gliosis and increasing radial glia and neural progenitor cells after spinal cord injury Brain Behav. 4 2014 187 200
57. G. Gowing, B. Shelley, K. Staggenborg, A. Hurley, P. Avalos, J. Victoroff, J. Latter, L. Garcia, and C.N. Svendsen Glial cell line-derived neurotrophic factor-secreting human neural progenitors show long-term survival, maturation into astrocytes, and no tumor formation following transplantation into the spinal cord of immunocompromised rats Neuroreport 25 2014 367 372
58. H. Gransee, W.Z. Zhan, G.C. Sieck, and C. Mantilla Localized delivery of BDNF-expressing mesenchymal stem cells enhances functional recovery following cervical spinal cord injury J. Neurotrauma. 2014 (EPub ahead of print)
59. R. Grill, K. Murai, A. Blesch, F.H. Gage, and M.H. Tuszynski Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury J. Neurosci. 17 1997 5560 5572
60. Y.L. Gu, L.W. Yin, Z. Zhang, J. Liu, S.J. Liu, L.F. Zhang, and T.H. Wang Neurotrophin expression in neural stem cells grafted acutely to transected spinal cord of adult rats linked to functional improvement Cell. Mol. Neurobiol. 32 2012 1089 1097
61. J.S. Guo, Y.S. Zeng, H.B. Li, W.L. Huang, R.Y. Liu, X.B. Li, Y. Ding, L.Z. Wu, and D.Z. Cai Cotransplant of neural stem cells and NT-3 gene modified Schwann cells promote the recovery of transected spinal cord injury Spinal Cord 45 2007 15 24
62. F.P. Guzen, J.G. Soares, L.M. de Freitas, J.R. Cavalcanti, F.G. Oliveira, J.F. Araujo, S. Cavalcante Jde, J.C. Cavalcante, E.S. do Nascimento, and M.S. de Oliveira Costa Jr. Sciatic nerve grafting and inoculation of FGF-2 promotes improvement of motor behavior and fiber regrowth in rats with spinal cord transection Restor. Neurol. Neurosci. 30 2012 265 275
63. T. Hagg, K.A. Baker, J.G. Emsley, and W. Tetzlaff Prolonged local neurotrophin-3 infusion reduces ipsilateral collateral sprouting of spared corticospinal axons in adult rats Neuroscience 130 2005 875 887
64. B.C. Hains, K.M. Johnson, M.J. Eaton, W.D. Willis, and C.E. Hulsebosch Serotonergic neural precursor cell grafts attenuate bilateral hyperexcitability of dorsal horn neurons after spinal hemisection in rat Neuroscience 116 2003 1097 1110
65. S. Han, B. Wang, W. Jin, Z. Xiao, B. Chen, H. Xiao, W. Ding, J. Cao, F. Ma, X. Li, B. Yuan, T. Zhu, X. Hou, J. Wang, J. Kong, W. Liang, and J. Dai The collagen scaffold with collagen binding BDNF enhances functional recovery by facilitating peripheral nerve infiltrating and ingrowth in canine complete spinal cord transection Spinal Cord 2014 (EPub ahead of print)
66. S.S. Hannila, and M.T. Filbin The role of cyclic amp signaling in promoting axonal regeneration after spinal cord injury Exp. Neurol. 209 2008 321 332
67. A.R. Harvey, and M.M. Tan Spontaneous regeneration of adult rat retinal ganglion cell axons in vivo Neuroreport 3 1992 239 242
68. A.R. Harvey, Y. Hu, S.G. Leaver, C.B. Mellough, K. Park, J. Verhaagen, G.W. Plant, and Q. Cui Gene therapy and transplantation in CNS repair: the visual system Prog. Retin. Eye Res. 25 2006 449 489
69. A.R. Harvey, J.W. Ooi, and J. Rodger Neurotrophic factors and the regeneration of adult retinal ganglion cell axons Int. Rev. Neurobiol. 106 2012 1 33
70. G.W. Hawryluk, A. Mothe, J. Wang, S. Wang, C. Tator, and M.G. Fehlings An in vivo characterization of trophic factor production following neural precursor cell or bone marrow stromal cell transplantation for spinal cord injury Stem Cells Dev. 21 2012 2222 2238
71. B.L. He, Y.C. Ba, X.Y. Wang, S.J. Liu, G.D. Liu, S. Ou, Y.L. Gu, X.H. Pan, and T.H. Wang BDNF expression with functional improvement in transected spinal cord treated with neural stem cells in adult rats Neuropeptides 47 2013 1 7
72. M. Hellström, and A.R. Harvey Retinal ganglion cell gene therapy and visual system repair Curr. Gene Ther. 11 2011 116 131
73. M. Hellström, and A.R. Harvey Cyclic AMP and the regeneration of retinal ganglion cell axons Int. J. Biochem. Cell Biol. 2014 S1357 S2725
74. G.W. Hiebert, K. Khodarahmi, J. McGraw, J.D. Steeves, and W. Tetzlaff Brain-derived neurotrophic factor applied to the motor cortex promotes sprouting of corticospinal fibers but not regeneration into a peripheral nerve transplant J. Neurosci. Res. 69 2002 160 168
75. E.R. Hollis 2nd, P. Lu, A. Blesch, and M.H. Tuszynski IGF-1 gene delivery promotes corticospinal neuronal survival but not regeneration after adult CNS injury Exp. Neurol. 215 2009 53 59
76. E.R. Hollis II, and M.H. Tuszynski Neurotrophins: potential therapeutic tools for the treatment of spinal cord injury Neurotherapeutics 8 2011 694 703
77. S. Hou, L. Nicholson, E. van Niekerk, M. Motsch, and A. Blesch Dependence of regenerated sensory axons on continuous neurotrophin-3 delivery J. Neurosci. 32 2012 13206 13220
78. M.T. Hougland, B.J. Harrison, D.S. Magnuson, E.C. Rouchka, and J.C. Petruska The transcriptional response of neurotrophins and their tyrosine kinase receptors in lumbar sensorimotor circuits to spinal cord contusion is affected by injury severity and survival time Front. Physiol. 3 2012 478
79. D.A. Houweling, A.J. Lankhorst, W.H. Gispen, P.R. Bar, and E.A. Joosten 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 1998 49 59
80. D.A. Houweling, J.T. van Asseldonk, A.J. Lankhorst, F.P. Hamers, D. Martin, P.R. Bar, and E.A. Joosten Local application of collagen containing brain-derived neurotrophic factor decreases the loss of function after spinal cord injury in the adult rat Neurosci. Lett. 251 1998 193 196
81. S.A. Hoyng, S. Gnavi, F. de Winter, R. Eggers, T. Ozawa, A. Zaldumbide, R.C. Hoeben, M.J. Malessy, and J. Verhaagen Developing a potentially immunologically inert tetracycline-regulatable viral vector for gene therapy in the peripheral nerve Gene Ther. 21 2014 549 557
82. E.J. Huang, and L.F. Reichardt Neurotrophins: roles in neuronal development and function Annu. Rev. Neurosci. 24 2001 677 736
83. F. Huang, J. Wang, and A. Chen Effects of co-grafts mesenchymal stem cells and nerve growth factor suspension in the repair of spinal cord injury J. Huazhong Univ. Sci. Technol. Med. Sci. 26 2006 206 210
84. W.C. Huang, H.S. Kuo, M.J. Tsai, H. Ma, C.W. Chiu, M.C. Huang, L.H. Yang, P.T. Chang, Y.L. Lin, W.C. Kuo, M.J. Lee, J.C. Liu, and H. Cheng Adeno-associated virus-mediated human acidic fibroblast growth factor expression promotes functional recovery of spinal cord-contused rats J. Gene Med. 13 2011 283 289
85. A.S. Hunanyan, H.A. Petrosyan, V. Alessi, and V.L. Arvanian Combination of chondroitinase ABC and AAV-NT3 promotes neural plasticity at descending spinal pathways after thoracic contusion in rats J. Neurophysiol. 110 2013 1782 1792
86. K.S. Hung, S.H. Tsai, T.C. Lee, J.W. Lin, C.K. Chang, and W.T. Chiu Gene transfer of insulin-like growth factor-1 providing neuroprotection after spinal cord injury in rats J. Neurosurg. Spine 6 2007 35 46
87. A. Hurtado, L.D. Moon, V. Maquet, B. Blits, R. Jerome, and M. Oudega Poly (d,l-lactic acid) macroporous guidance scaffolds seeded with schwann cells genetically modified to secrete a bi-functional neurotrophin implanted in the completely transected adult rat thoracic spinal cord Biomaterials 27 2006 430 442
88. D.H. Hwang, H.M. Kim, Y.M. Kang, I.S. Joo, C.S. Cho, B.W. Yoon, S.U. Kim, and B.G. Kim Combination of multifaceted strategies to maximize the therapeutic benefits of neural stem cell transplantation for spinal cord repair Cell Transplant. 20 2011 1361 1379
89. C. Iannotti, H. Li, P. Yan, X. Lu, L. Wirthlin, and X.M. Xu Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury Exp. Neurol. 183 2003 379 393
90. C. Iannotti, Y. Ping Zhang, C.B. Shields, Y. Han, D.A. Burke, and X.M. Xu A neuroprotective role of glial cell line-derived neurotrophic factor following moderate spinal cord contusion injury Exp. Neurol. 189 2004 317 332
91. D.E. Iarikov, B.G. Kim, H.N. Dai, M. McAtee, P.L. Kuhn, and B.S. Bregman Delayed transplantation with exogenous neurotrophin administration enhances plasticity of corticofugal projections after spinal cord injury J. Neurotrauma 24 2007 690 702
92. N.Y. Ip, J. McClain, N.X. Barrezueta, T.H. Aldrich, L. Pan, Y. Li, S.J. Wiegand, B. Friedman, S. Davis, and G.D. Yancopoulos The alpha component of the CNTF receptor is required for signaling and defines potential CNTF targets in the adult and during development Neuron 10 1993 89 102
93. K. Ishii, M. Nakamura, H. Dai, T.P. Finn, H. Okano, Y. Toyama, and B.S. Bregman Neutralization of ciliary neurotrophic factor reduces astrocyte production from transplanted neural stem cells and promotes regeneration of corticospinal tract fibers in spinal cord injury J. Neurosci. Res. 84 2006 1669 1681
94. A. Jain, Y.T. Kim, R.J. McKeon, and R.V. Bellamkonda In situ gelling hydrogels for conformal repair of spinal cord defects, and local delivery of BDNF after spinal cord injury Biomaterials 27 2006 497 504
95. A. Jain, R.J. McKeon, S.M. Brady-Kalnay, and R.V. Bellamkonda Sustained delivery of activated Rho GTPases and BDNF promotes axon growth in CSPG-rich regions following spinal cord injury PloS One 6 2011 e16135
96. Y. Jin, I. Fischer, A. Tessler, and J.D. Houle 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
97. P.J. Johnson, A. Tatara, D.A. McCreedy, A. Shiu, and S.E. Sakiyama-Elbert Tissue-engineered fibrin scaffolds containing neural progenitors enhance functional recovery in a subacute model of SCI Soft Matter 6 2010 5127 5137
98. P.J. Johnson, A. Tatara, A. Shiu, and S.E. Sakiyama-Elbert Controlled release of neurotrophin-3 and platelet-derived growth factor from fibrin scaffolds containing neural progenitor cells enhances survival and differentiation into neurons in a subacute model of SCI Cell Transplant. 19 2010 89 101
99. M.S. Joseph, N.J. Tillakaratne, and R.D. de Leon Treadmill training stimulates brain-derived neurotrophic factor mRNA expression in motor neurons of the lumbar spinal cord in spinally transected rats Neuroscience 224 2012 135 144
100. K. Kadoya, S. Tsukada, P. Lu, G. Coppola, D. Geschwind, M.T. Filbin, A. Blesch, and M.H. Tuszynski Combined intrinsic and extrinsic neuronal mechanisms facilitate bridging axonal regeneration one year after spinal cord injury Neuron 64 2009 165 172
101. C.E. Kang, M.D. Baumann, C.H. Tator, and M.S. Shoichet Localized and sustained delivery of fibroblast growth factor-2 from a nanoparticle-hydrogel composite for treatment of spinal cord injury Cells Tissues Organs 197 2013 55 63
102. H. Kanno, Y. Pressman, A. Moody, R. Berg, E.M. Muir, J.H. Rogers, H. Ozawa, E. Itoi, D.D. Pearse, and M.B. Bunge Combination of engineered Schwann cell grafts to secrete neurotrophin and chondroitinase promotes axonal regeneration and locomotion after spinal cord injury J. Neurosci. 34 2014 1838 1855
103. S. Karimi-Abdolrezaee, E. Eftekharpour, J. Wang, D. Schut, and M.G. Fehlings Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord J. Neurosci. 30 2010 1657 1676
104. M. Kasai, T. Jikoh, H. Fukumitsu, and S. Furukawa FGF-2-responsive and spinal cord-resident cells improve locomotor function after spinal cord injury J. Neurotrauma 31 18 2014 1584 1598
105. B.J. Kerr, E.J. Bradbury, D.L. Bennett, P.M. Trivedi, P. Dassan, J. French, D.B. Shelton, S.B. McMahon, and S.W. Thompson Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord J. Neurosci. 19 1999 5138 5148
106. K.A. Kigerl, V.M. McGaughy, and P.G. Popovich Comparative analysis of lesion development and intraspinal inflammation in four strains of mice following spinal contusion injury J. Comp. Neurol. 494 2006 578 594
107. K.N. Kim, S.H. Oh, K.H. Lee, and D.H. Yoon Effect of human mesenchymal stem cell transplantation combined with growth factor infusion in the repair of injured spinal cord Acta Neurochir. Suppl. 99 2006 133 136
108. V.R. King, E.J. Bradbury, S.B. McMahon, and J.V. Priestley Changes in truncated Trkb and p75 receptor expression in the rat spinal cord following spinal cord hemisection and spinal cord hemisection plus neurotrophin treatment Exp. Neurol. 165 2000 327 341
109. M.C. Klaw, C. Xu, and V.J. Tom Intraspinal AAV injections immediately rostral to a thoracic spinal cord injury site efficiently transduces neurons in spinal cord and brain Mol. Ther. Nucleic Acids 2 2013 e108
110. N.R. Kobayashi, D.P. Fan, K.M. Giehl, A.M. Bedard, S.J. Wiegand, and W. Tetzlaff BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and Talpha1-tubulin mRNA expression, and promote axonal regeneration J. Neurosci. 17 1997 9583 9595
111. M. Koda, M. Hashimoto, M. Murakami, K. Yoshinaga, O. Ikeda, M. Yamazaki, S. Koshizuka, T. Kamada, H. Moriya, H. Shirasawa, S. Sakao, and H. Ino Adenovirus vector-mediated in vivo gene transfer of brain-derived neurotrophic factor (BDNF) promotes rubrospinal axonal regeneration and functional recovery after complete transection of the adult rat spinal cord J. Neurotrauma 21 2004 329 337
112. M. Koda, T. Kamada, M. Hashimoto, M. Murakami, H. Shirasawa, S. Sakao, H. Ino, K. Yoshinaga, S. Koshizuka, H. Moriya, and M. Yamazaki Adenovirus vector-mediated ex vivo gene transfer of brain-derived neurotrophic factor to bone marrow stromal cells promotes axonal regeneration after transplantation in completely transected adult rat spinal cord Eur. Spine J. 16 2007 2206 2214
113. A. Kojima, and C.H. Tator Intrathecal administration of epidermal growth factor and fibroblast growth factor 2 promotes ependymal proliferation and functional recovery after spinal cord injury in adult rats J. Neurotrauma 19 2002 223 238
114. Y. Kovalchuk, K. Holthoff, and A. Konnerth Neurotrophin action on a rapid timescale Curr. Opin. Neurobiol. 14 2004 558 563
115. T. Kurimoto, Y. Yin, K. Omura, H.Y. Gilbert, D. Kim, L.P. Cen, L. Moko, S. Kugler, and L.I. Benowitz Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, camp, and pten gene deletion J. Neurosci. 30 2010 15654 15663
116. K. Kusano, M. Enomoto, T. Hirai, P. Tsoulfas, S. Sotome, K. Shinomiya, and A. Okawa Transplanted neural progenitor cells expressing mutant NT3 promote myelination and partial hindlimb recovery in the chronic phase after spinal cord injury Biochem. Biophys. Res. Commun. 393 2010 812 817
117. B.K. Kwon, J. Liu, C. Messerer, N.R. Kobayashi, J. McGraw, L. Oschipok, and W. Tetzlaff Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury Proc. Natl. Acad. Sci. USA 99 2002 3246 3251
118. B.K. Kwon, J. Liu, L. Oschipok, J. Teh, Z.W. Liu, and W. Tetzlaff Rubrospinal neurons fail to respond to brain-derived neurotrophic factor applied to the spinal cord injury site 2 months after cervical axotomy Exp. Neurol. 189 2004 45 57
119. B.K. Kwon, J. Liu, C. Lam, W. Plunet, L.W. Oschipok, W. Hauswirth, A. Di Polo, A. Blesch, and W. Tetzlaff Brain-derived neurotrophic factor gene transfer with adeno-associated viral and lentiviral vectors prevents rubrospinal neuronal atrophy and stimulates regeneration-associated gene expression after acute cervical spinal cord injury Spine 32 2007 1164 1173
120. S.G. Leaver, Q. Cui, G.W. Plant, A. Arulpragasam, S. Hisheh, J. Verhaagen, and A.R. Harvey AAV-mediated expression of cntf promotes long-term survival and regeneration of adult rat retinal ganglion cells Gene Ther. 13 2006 1328 1341
121. H. Lee, M.H. Jin, H.J. Kang, C.H. Hong, W.J. Bang, K.K. Park, and S.W. Han Timing of prepubertal androgen administration may have different effects on future fertility as well as penile size in normal male rats Urology 75 2010 979 984
122. M.J. Lee, C.J. Chen, C.H. Cheng, W.C. Huang, H.S. Kuo, J.C. Wu, M.J. Tsai, M.C. Huang, W.C. Chang, and H. Cheng Combined treatment using peripheral nerve graft and FGF-1: Changes to the glial environment and differential macrophage reaction in a complete transected spinal cord Neurosci. Lett. 433 2008 163 169
123. M.Y. Lee, C.J. Kim, S.L. Shin, S.H. Moon, and M.H. Chun Increased ciliary neurotrophic factor expression in reactive astrocytes following spinal cord injury in the rat Neurosci. Lett. 255 1998 79 82
124. T.T. Lee, B.A. Green, W.D. Dietrich, and R.P. Yezierski Neuroprotective effects of basic fibroblast growth factor following spinal cord contusion injury in the rat J. Neurotrauma 16 1999 347 356
125. V.P. Lemmon, S. Abeyruwan, U. Visser, and J.L. Bixby Facilitating transparency in spinal cord injury studies using data standards and ontologies Neural Regen. Res. 9 2014 6 7
126. V.P. Lemmon, A.R. Ferguson, P.G. Popovich, X.M. Xu, D.M. Snow, M. Igarashi, C.E. Beattie, and J.L. Bixby Minimum information about a spinal cord injury experiment: a proposed reporting standard for spinal cord injury experiments J. Neurotrauma 2014
127. D.J. Liebl, W. Huang, W. Young, and L.F. Parada Regulation of trk receptors following contusion of the rat spinal cord Exp. Neurol. 167 2001 15 26
128. P. Lingor, L. Tonges, N. Pieper, C. Bermel, E. Barski, V. Planchamp, and M. Bahr Rock inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells Brain 131 2008 250 263
129. K. Liu, Y. Lu, J.K. Lee, R. Samara, R. Willenberg, I. Sears-Kraxberger, A. Tedeschi, K.K. Park, D. Jin, B. Cai, B. Xu, L. Connolly, O. Steward, B. Zheng, and Z. He PTEN deletion enhances the regenerative ability of adult corticospinal neurons Nat. Neurosci. 13 2010 1075 1081
130. Y. Liu, D. Kim, B.T. Himes, S.Y. Chow, T. Schallert, M. Murray, A. Tessler, and I. Fischer Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function J. Neurosci. 19 1999 4370 4387
131. P. Lu, A. Blesch, and M.H. Tuszynski Neurotrophism without neurotropism: BDNF promotes survival but not growth of lesioned corticospinal neurons J. Comp. Neurol. 436 2001 456 470
132. P. Lu, H. Yang, L.L. Jones, M.T. Filbin, and M.H. Tuszynski Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury J. Neurosci. 24 2004 6402 6409
133. P. Lu, L.L. Jones, and M.H. Tuszynski BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury Exp. Neurol. 191 2005 344 360
134. P. Lu, L.L. Jones, and M.H. Tuszynski Axon regeneration through scars and into sites of chronic spinal cord injury Exp. Neurol. 203 2007 8 21
135. P. Lu, and M.H. Tuszynski Growth factors and combinatorial therapies for CNS regeneration Exp. Neurol. 209 2008 313 320
136. P. Lu, Y. Wang, L. Graham, K. McHale, M. Gao, D. Wu, J. Brock, A. Blesch, E.S. Rosenzweig, L.A. Havton, B. Zheng, J.M. Conner, M. Marsala, and M.H. Tuszynski Long-distance growth and connectivity of neural stem cells after severe spinal cord injury Cell 150 2012 1264 1273
137. P. Lu, G. Woodruff, Y. Wang, L. Graham, M. Hunt, D. Wu, E. Boehle, R. Ahmad, G. Poplawski, J. Brock, L.S. Goldstein, and M.H. Tuszynski Long-distance axonal growth from human induced pluripotent stem cells after spinal cord injury Neuron 83 2014 789 796
138. X. Luo, and K.K. Park Neuron-intrinsic inhibitors of axon regeneration: Pten and SOCS3 Int. Rev. Neurobiol. 105 2012 141 173
139. J.V. Lynskey, F.A. Sandhu, H.N. Dai, M. McAtee, J.R. Slotkin, L. MacArthur, and B.S. Bregman Delayed intervention with transplants and neurotrophic factors supports recovery of forelimb function after cervical spinal cord injury in adult rats J. Neurotrauma 23 2006 617 634
140. M.Y. Macias, M.B. Syring, M.A. Pizzi, M.J. Crowe, A.R. Alexanian, and S.N. Kurpad Pain with no gain: allodynia following neural stem cell transplantation in spinal cord injury Exp. Neurol. 201 2006 335 348
141. C.B. Mantilla, H.M. Gransee, W.Z. Zhan, and G.C. Sieck Motoneuron BDNF/Trkb signaling enhances functional recovery after cervical spinal cord injury Exp. Neurol. 247 2013 101 109
142. J. McCall, N. Weidner, and A. Blesch Neurotrophic factors in combinatorial approaches for spinal cord regeneration Cell Tissue Res. 349 2012 27 37
143. D.M. McTigue, P.J. Horner, B.T. Stokes, and F.H. Gage Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord J. Neurosci. 18 1998 5354 5365
144. M.F. Meijs, L. Timmers, D.D. Pearse, P.A. Tresco, M.L. Bates, E.A. Joosten, M.B. Bunge, and M. Oudega Basic fibroblast growth factor promotes neuronal survival but not behavioral recovery in the transected and Schwann cell implanted rat thoracic spinal cord J. Neurotrauma 21 2004 1415 1430
145. P. Menei, C. Montero-Menei, S.R. Whittemore, R.P. Bunge, and M.B. Bunge Schwann cells genetically modified to secrete human bdnf promote enhanced axonal regrowth across transected adult rat spinal cord Eur. J. Neurosci. 10 1998 607 621
146. X.T. Meng, C. Li, Z.Y. Dong, J.M. Liu, W. Li, Y. Liu, H. Xue, and D. Chen Co-transplantation of bFGF-expressing amniotic epithelial cells and neural stem cells promotes functional recovery in spinal cord-injured rats Cell Biol. Int. 32 2008 1546 1558
147. P.K. Menon, D.F. Muresanu, A. Sharma, H. Mossler, and H.S. Sharma Cerebrolysin, a mixture of neurotrophic factors induces marked neuroprotection in spinal cord injury following intoxication of engineered nanoparticles from metals CNS Neurol. Disord. Drug Targets 11 2012 40 49
148. B.D.t. Moore, C.W. Kiley, C. Sun, and W.M. Usrey Rapid plasticity of visual responses in the adult lateral geniculate nucleus Neuron 71 2011 812 819
149. M. Nakamura, and B.S. Bregman Differences in neurotrophic factor gene expression profiles between neonate and adult rat spinal cord after injury Exp. Neurol. 169 2001 407 415
150. L.N. Novikova, L.N. Novikov, and J.O. Kellerth 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
151. K. Ollivier-Lanvin, I. Fischer, V. Tom, J.D. Houle, and M.A. Lemay Either brain-derived neurotrophic factor or neurotrophin-3 only neurotrophin-producing grafts promote locomotor recovery in untrained spinalized cats Neurorehabil. Neural Repair 2014 (Epub ahead of print)
152. M. Oudega, X.M. Xu, V. Guenard, N. Kleitman, and M.B. Bunge A combination of insulin-like growth factor-1 and platelet-derived growth factor enhances myelination but diminishes axonal regeneration into Schwann cell grafts in the adult rat spinal cord Glia 19 1997 247 258
153. M. Oudega, E.J. Bradbury, and M.S. Ramer Combination therapies Handb. Clin. Neurol. 109 2012 617 636
154. P.H. Ozdinler, and J.D. Macklis IGF-1 specifically enhances axon outgrowth of corticospinal motor neurons Nat. Neurosci. 9 2006 1371 1381
155. K.K. Park, K. Liu, Y. Hu, P.D. Smith, C. Wang, B. Cai, B. Xu, L. Connolly, I. Kramvis, M. Sahin, and Z. He Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway Science 322 2008 963 966
156. K.K. Park, Y. Hu, J. Muhling, M.A. Pollett, E.J. Dallimore, A.M. Turnley, Q. Cui, and A.R. Harvey Cytokine-induced SOCS expression is inhibited by cAMP analogue: impact on regeneration in injured retina Mol. Cell. Neurosci. 41 2009 313 324
157. A.G. Peace, and D.A. Shewan New perspectives in cyclic AMP-mediated axon growth and guidance: the emerging epoch of Epac Brain Res. Bull. 84 2011 280 288
158. D.D. Pearse, F.C. Pereira, A.E. Marcillo, M.L. Bates, Y.A. Berrocal, M.T. Filbin, and M.B. Bunge cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury Nat. Med. 10 2004 610 616
159. J. Piantino, J.A. Burdick, D. Goldberg, R. Langer, and L.I. Benowitz An injectable, biodegradable hydrogel for trophic factor delivery enhances axonal rewiring and improves performance after spinal cord injury Exp. Neurol. 201 2006 359 367
160. J.R. Plemel, M.B. Keough, G.J. Duncan, J.S. Sparling, V.W. Yong, P.K. Stys, and W. Tetzlaff Remyelination after spinal cord injury: is it a target for repair? Prog. Neurobiol. 117 2014 54 72
161. D.X. Qin, X.L. Zou, W. Luo, W. Zhang, H.T. Zhang, X.L. Li, H. Zhang, X.Y. Wang, and T.H. Wang Expression of some neurotrophins in the spinal motoneurons after cord hemisection in adult rats Neurosci. Lett. 410 2006 222 227
162. A.G. Rabchevsky, I. Fugaccia, A. Fletcher-Turner, D.A. Blades, M.P. Mattson, and S.W. Scheff Basic fibroblast growth factor (bFGF) enhances tissue sparing and functional recovery following moderate spinal cord injury J. Neurotrauma 16 1999 817 830
163. J. Rodger, E.S. Drummond, M. Hellström, D. Robertson, and A.R. Harvey Long-term gene therapy causes transgene-specific changes in the morphology of regenerating retinal ganglion cells PloS One 7 2012 e31061
164. M.I. Romero, N. Rangappa, M.G. Garry, and G.M. Smith Functional regeneration of chronically injured sensory afferents into adult spinal cord after neurotrophin gene therapy J. Neurosci. 21 2001 8408 8416
165. M.J. Ruitenberg, G.W. Plant, F.P. Hamers, J. Wortel, B. Blits, P.A. Dijkhuizen, W.H. Gispen, G.J. Boer, and J. Verhaagen Ex vivo adenoviral vector-mediated neurotrophin gene transfer to olfactory ensheathing glia: effects on rubrospinal tract regeneration, lesion size, and functional recovery after implantation in the injured rat spinal cord J. Neurosci. 23 2003 7045 7058
166. M.J. Ruitenberg, B. Blits, P.A. Dijkhuizen, E.T. te Beek, A. Bakker, J.J. van Heerikhuize, C.W. Pool, W.T. Hermens, G.J. Boer, and J. Verhaagen Adeno-associated viral vector-mediated gene transfer of brain-derived neurotrophic factor reverses atrophy of rubrospinal neurons following both acute and chronic spinal cord injury Neurobiol. Dis. 15 2004 394 406
167. M.J. Ruitenberg, D.B. Levison, S.V. Lee, J. Verhaagen, A.R. Harvey, and G.W. Plant NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration Brain 128 2005 839 853
168. S. Sakiyama-Elbert, P.J. Johnson, S.I. Hodgetts, G.W. Plant, and A.R. Harvey Scaffolds to promote spinal cord regeneration Handb. Clin. Neurol. 109 2012 575 594
169. M. Sasaki, C. Radtke, A.M. Tan, P. Zhao, H. Hamada, K. Houkin, O. Honmou, and J.D. Kocsis BDNF-hypersecreting human mesenchymal stem cells promote functional recovery, axonal sprouting, and protection of corticospinal neurons after spinal cord injury J. Neurosci. 29 2009 14932 14941
170. L. Schnell, R. Schneider, R. Kolbeck, Y.A. Barde, and M.E. Schwab Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion Nature 367 1994 170 173
171. L. Schnell, A.S. Hunanyan, W.J. Bowers, P.J. Horner, H.J. Federoff, M. Gullo, M.E. Schwab, L.M. Mendell, and V.L. Arvanian Combined delivery of Nogo-A antibody, neurotrophin-3 and the NMDA-NR2d subunit establishes a functional 'detour' in the hemisected spinal cord Eur. J. Neurosci. 34 2011 1256 1267
172. M.E. Schwab, and S.M. Strittmatter Nogo limits neural plasticity and recovery from injury Curr. Opin. Neurobiol. 27C 2014 53 60
173. K.G. Sharp, L.A. Flanagan, K.M. Yee, and O. Steward A re-assessment of a combinatorial treatment involving Schwann cell transplants and elevation of cyclic AMP on recovery of motor function following thoracic spinal cord injury in rats Exp. Neurol. 233 2012 625 644
174. D.A. Shin, W.A. Pennant, H. Yoon do, Y. Ha, and K.N. Kim Co-transplantation of bone marrow-derived mesenchymal stem cells and nanospheres containing FGF-2 improve cell survival and neurological function in the injured rat spinal cord Acta Neurochir. 156 2014 297 303
175. U. Slawinska, K. Miazga, and L.M. Jordan The role of serotonin in the control of locomotor movements and strategies for restoring locomotion after spinal cord injury Acta Neurobiol. Exp. (Wars) 74 2014 172 187
176. G.M. Smith, A.E. Falone, and E. Frank Sensory axon regeneration: rebuilding functional connections in the spinal cord Trends Neurosci. 35 2012 156 163
177. M.T. Sommerfeld, R. Schweigreiter, Y.A. Barde, and E. Hoppe Down-regulation of the neurotrophin receptor Trkb following ligand binding. Evidence for an involvement of the proteasome and differential regulation of Trka and Trkb J. Biol. Chem. 275 2000 8982 8990
178. O. Steward, P.G. Popovich, W.D. Dietrich, and N. Kleitman Replication and reproducibility in spinal cord injury research Exp. Neurol. 233 2012 597 605
179. S. Stokols, J. Sakamoto, C. Breckon, T. Holt, J. Weiss, and M.H. Tuszynski Templated agarose scaffolds support linear axonal regeneration Tissue Eng. 12 2006 2777 2787
180. F. Sun, and Z. He Neuronal intrinsic barriers for axon regeneration in the adult CNS Curr. Opin. Neurobiol. 20 2010 510 518
181. L. Taylor, L. Jones, M.H. Tuszynski, and A. Blesch Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord J. Neurosci. 26 2006 9713 9721
182. S.J. Taylor, E.S. Rosenzweig, J.W. McDonald III, and S.E. Sakiyama-Elbert Delivery of neurotrophin-3 from fibrin enhances neuronal fiber sprouting after spinal cord injury J. Control Release 113 2006 226 235
183. W. Tetzlaff, E.B. Okon, S. Karimi-Abdolrezaee, C.E. Hill, J.S. Sparling, J.R. Plemel, W.T. Plunet, E.C. Tsai, D. Baptiste, L.J. Smithson, M.D. Kawaja, M.G. Fehlings, and B.K. Kwon A systematic review of cellular transplantation therapies for spinal cord injury J. Neurotrauma 28 2011 1611 1682
184. A.M. Thomas, S.K. Seidlits, A.G. Goodman, T.V. Kukushliev, D.M. Hassani, B.J. Cummings, A.J. Anderson, and L.D. Shea Sonic hedgehog and neurotrophin-3 increase oligodendrocyte numbers and myelination after spinal cord injury Integr. Biol. (Cambridge) 6 2014 694 705
185. C.A. Tobias, N.O. Dhoot, M.A. Wheatley, A. Tessler, M. Murray, and I. Fischer Grafting of encapsulated BDNF-producing fibroblasts into the injured spinal cord without immune suppression in adult rats J. Neurotrauma 18 2001 287 301
186. C.A. Tobias, S.S. Han, J.S. Shumsky, D. Kim, M. Tumolo, N.O. Dhoot, M.A. Wheatley, I. Fischer, A. Tessler, and M. Murray Alginate encapsulated BDNF-producing fibroblast grafts permit recovery of function after spinal cord injury in the absence of immune suppression J. Neurotrauma 22 2005 138 156
187. V.J. Tom, H.R. Sandrow-Feinberg, K. Miller, L. Santi, T. Connors, M.A. Lemay, and J.D. Houle Combining peripheral nerve grafts and chondroitinase promotes functional axonal regeneration in the chronically injured spinal cord J. Neurosci. 29 2009 14881 14890
188. V.J. Tom, H.R. Sandrow-Feinberg, K. Miller, C. Domitrovich, J. Bouyer, V. Zhukareva, M.C. Klaw, M.A. Lemay, and J.D. Houle Exogenous BDNF enhances the integration of chronically injured axons that regenerate through a peripheral nerve grafted into a chondroitinase-treated spinal cord injury site Exp. Neurol. 239 2013 91 100
189. R.B. Tripathi, and D.M. McTigue Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats J. Comp. Neurol. 510 2008 129 144
190. E.C. Tsai, P.D. Dalton, M.S. Shoichet, and C.H. Tator Matrix inclusion within synthetic hydrogel guidance channels improves specific supraspinal and local axonal regeneration after complete spinal cord transection Biomaterials 27 2006 519 533
191. M.C. Tsai, L.F. Shen, H.S. Kuo, H. Cheng, and K.F. Chak Involvement of acidic fibroblast growth factor in spinal cord injury repair processes revealed by a proteomics approach Mol. Cell. Proteomics 7 2008 1668 1687
192. H.M. Tuinstra, M.O. Aviles, S. Shin, S.J. Holland, M.L. Zelivyanskaya, A.G. Fast, S.Y. Ko, D.J. Margul, A.K. Bartels, R.M. Boehler, B.J. Cummings, A.J. Anderson, and L.D. Shea Multifunctional, multichannel bridges that deliver neurotrophin encoding lentivirus for regeneration following spinal cord injury Biomaterials 33 2012 1618 1626
193. M.H. Tuszynski, D.A. Peterson, J. Ray, A. Baird, Y. Nakahara, and F.H. Gage Fibroblasts genetically modified to produce nerve growth factor induce robust neuritic ingrowth after grafting to the spinal cord Exp. Neurol. 126 1994 1 14
194. M.H. Tuszynski, K. Murai, A. Blesch, R. Grill, and I. Miller Functional characterization of NGF-secreting cell grafts to the acutely injured spinal cord Cell Transplant. 6 1997 361 368
195. M.H. Tuszynski, N. Weidner, M. McCormack, I. Miller, H. Powell, and J. Conner Grafts of genetically modified Schwann cells to the spinal cord: survival, axon growth, and myelination Cell Transplant. 7 1998 187 196
196. M.H. Tuszynski, R. Grill, L.L. Jones, H.M. McKay, and A. Blesch Spontaneous and augmented growth of axons in the primate spinal cord: effects of local injury and nerve growth factor-secreting cell grafts J. Comp. Neurol. 449 2002 88 101
197. R. Urfer, P. Tsoulfas, D. Soppet, E. Escandon, L.F. Parada, and L.G. Presta The binding epitopes of neurotrophin-3 to its receptors Trkc and gp75 and the design of a multifunctional human neurotrophin EMBO J. 13 1994 5896 5909
198. R. Vavrek, J. Girgis, W. Tetzlaff, G.W. Hiebert, and K. Fouad Bdnf promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats Brain 129 2006 1534 1545
199. J. Vukovic, G.W. Plant, M.J. Ruitenberg, and A.R. Harvey Influence of adult schwann cells and olfactory ensheathing glia on axon-target cell interactions in the CNS: a comparative analysis using a retinotectal co-graft model Neuron Glia Biol. 3 2007 105 117
200. L.J. Wang, R.P. Zhang, and J.D. Li Transplantation of neurotrophin-3-expressing bone mesenchymal stem cells improves recovery in a rat model of spinal cord injury Acta Neurochir. 156 2014 1409 1418
201. N. Weidner, A. Blesch, R.J. Grill, and M.H. Tuszynski Nerve growth factor-hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1 J. Comp. Neurol. 413 1999 495 506
202. N. Weishaupt, A. Blesch, and K. Fouad BDNF: the career of a multifaceted neurotrophin in spinal cord injury Exp. Neurol. 238 2012 254 264
203. N. Weishaupt, S. Li, A. Di Pardo, S. Sipione, and K. Fouad Synergistic effects of BDNF and rehabilitative training on recovery after cervical spinal cord injury Behav. Brain Res. 239 2013 31 42
204. N. Weishaupt, A.L. Mason, C. Hurd, Z. May, D.C. Zmyslowski, D. Galleguillos, S. Sipione, and K. Fouad Vector-induced NT-3 expression in rats promotes collateral growth of injured corticospinal tract axons far rostral to a spinal cord injury Neuroscience 272 2014 65 75
205. H.R. Widmer, D.R. Kaplan, S.J. Rabin, K.D. Beck, F. Hefti, and B. Knusel Rapid phosphorylation of phospholipase C gamma 1 by brain-derived neurotrophic factor and neurotrophin-3 in cultures of embryonic rat cortical neurons J. Neurochem. 60 1993 2111 2123
206. I. Wong, H. Liao, X. Bai, A. Zaknic, J. Zhong, Y. Guan, H.Y. Li, Y.J. Wang, and X.F. Zhou ProBDNF inhibits infiltration of ED1+ macrophages after spinal cord injury Brain Behav. Immun. 24 2010 585 597
207. J.C. Wu, W.C. Huang, Y.A. Tsai, Y.C. Chen, and H. Cheng Nerve repair using acidic fibroblast growth factor in human cervical spinal cord injury: a preliminary phase i clinical study J. Neurosurg. Spine 8 2008 208 214
208. X.M. Xu, V. Guenard, N. Kleitman, P. Aebischer, and M.B. Bunge A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord Exp. Neurol. 134 1995 261 272
209. J. Ye, L. Cao, R. Cui, A. Huang, Z. Yan, C. Lu, and C. He The effects of ciliary neurotrophic factor on neurological function and glial activity following contusive spinal cord injury in the rats Brain Res. 997 2004 30 39
210. L.W. Yick, W. Wu, K.F. So, and H.K. Yip Peripheral nerve graft and neurotrophic factors enhance neuronal survival and expression of nitric oxide synthase in Clarke's nucleus after hemisection of the spinal cord in adult rat Exp. Neurol. 159 1999 131 138
211. F. Yin, P. Li, M. Zheng, L. Chen, Q. Xu, K. Chen, Y.Y. Wang, Y.Y. Zhang, and C. Han Interleukin-6 family of cytokines mediates isoproterenol-induced delayed STAT3 activation in mouse heart J. Biol. Chem. 278 2003 21070 21075
212. Z. Ying, R.R. Roy, V.R. Edgerton, and F. Gomez-Pinilla Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury Exp. Neurol. 193 2005 411 419
213. L.J. Zai, S. Yoo, and J.R. Wrathall Increased growth factor expression and cell proliferation after contusive spinal cord injury Brain Res. 1052 2005 147 155
214. A. Zaldumbide, S. Weening, S.J. Cramer, M.J. Rabelink, J. Verhaagen, and R.C. Hoeben A potentially immunologically inert derivative of the reverse tetracycline-controlled transactivator Biotechnol. Lett. 32 2010 749 754
215. H. Zhang, F. Wu, X. Kong, J. Yang, H. Chen, L. Deng, Y. Cheng, L. Ye, S. Zhu, X. Zhang, Z. Wang, H. Shi, X. Fu, X. Li, H. Xu, L. Lin, and J. Xiao Nerve growth factor improves functional recovery by inhibiting endoplasmic reticulum stress-induced neuronal apoptosis in rats with spinal cord injury J. Transl. Med. 12 2014 130
216. L. Zhang, Z. Ma, G.M. Smith, X. Wen, Y. Pressman, P.M. Wood, and X.M. Xu GDNF-enhanced axonal regeneration and myelination following spinal cord injury is mediated by primary effects on neurons Glia 57 2009 1178 1191
217. T. Zhao, W. Yan, K. Xu, Y. Qi, X. Dai, and Z. Shi Combined treatment with platelet-rich plasma and brain-derived neurotrophic factor-overexpressing bone marrow stromal cells supports axonal remyelination in a rat spinal cord hemi-section model Cytotherapy 15 2013 792 804
218. L. Zhou, and H.D. Shine Neurotrophic factors expressed in both cortex and spinal cord induce axonal plasticity after spinal cord injury J. Neurosci. Res. 74 2003 221 226
219. E. Ziemlinska, S. Kugler, M. Schachner, I. Wewior, J. Czarkowska-Bauch, and M. Skup Overexpression of BDNF increases excitability of the lumbar spinal network and leads to robust early locomotor recovery in completely spinalized rats PloS One 9 2014 e88833
220. K. Zukor, S. Belin, C. Wang, N. Keelan, X. Wang, and Z. He Short hairpin RNA against PTEN enhances regenerative growth of corticospinal tract axons after spinal cord injury J. Neurosci. 33 2013 15350 15361