Neurotrophic factors and the regeneration of adult retinal ganglion cell axons

International Review of Neurobiology

Volumn 106, Issue , 2012, Pages 1-33

  Harvey, Alan R ^a   Ooi, Jacob Wei Wei ^a   Rodger, Jennifer ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Brain derived neurotrophic factor; Ciliary neurotrophic factor; Gene therapy; Neurotrophins; Optic nerve; Optic tract; Peripheral nerve grafts; Retinal ganglion cells

Indexed keywords

8 (4 CHLOROPHENYLTHIO) CYCLIC AMP; ADENOVIRUS VECTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CILIARY NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FORSKOLIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LENTIVIRUS VECTOR; LEUKEMIA INHIBITORY FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN 4; PARVOVIRUS VECTOR; RECOMBINANT BRAIN DERIVED NEUROTROPHIC FACTOR; RECOMBINANT CILIARY NEUROTROPHIC FACTOR; SCATTER FACTOR; SOMATOMEDIN C; SUPPRESSOR OF CYTOKINE SIGNALING 3; VIRUS VECTOR;

ARTICLE; CELL ENCAPSULATION; CELL SURVIVAL; CELL SUSPENSION; CELL VIABILITY; ELECTROPORATION; MESENCHYMAL STEM CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GRAFT; NERVE SPROUTING; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; OPTIC NERVE INJURY; OPTIC TRACT; PRIORITY JOURNAL; RETINA GANGLION CELL; SCHWANN CELL; SIGNAL TRANSDUCTION; SUPERIOR COLLICULUS; VIRAL GENE DELIVERY SYSTEM; VISUAL SYSTEM;

EID: 84870512887     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407178-0.00002-8     Document Type: Chapter

References (174)

1. Ahmed Z., Berry M., Logan A. ROCK inhibition promotes adult retinal ganglion cell neurite outgrowth only in the presence of growth promoting factors. Molecular and Cellular Neuroscience 2009, 42:128-133.
2. Ahmed Z., Suggate E.L., Brown E.R., Dent R.G., Armstrong S.J., Barrett L.B., et al. Schwann cell-derived factor-induced modulation of the NgR/p75NTR/EGFR axis disinhibits axon growth through CNS myelin in vivo and in vitro. Brain 2006, 129:1517-1533.
3. Alabed Y.Z., Pool M., Ong Tone S., Sutherland C., Fournier A.E. GSK3 beta regulates myelin-dependent axon outgrowth inhibition through CRMP4. The Journal of Neuroscience 2010, 30:5635-5643.
4. Andrieu-Soler C., Bejjani R.A., de Bizemont T., Normand N., BenEzra D., Behar-Cohen F. Ocular gene therapy: A review of nonviral strategies. Molecular Vision 2006, 12:1334-1347.
5. Bai Y., Dergham P., Nedev H., Xu J., Galan A., Rivera J.C., et al. Chronic and acute models of retinal neurodegeneration TrkA activity are neuroprotective whereas p75NTR activity is neurotoxic through a paracrine mechanism. The Journal of Biological Chemistry 2010, 285:39392-39400.
6. Bai Y., Shi Z., Zhuo Y., Liu J., Malakhov A., Ko E., et al. In glaucoma the upregulated truncated TrkC.T1 receptor isoform in glia causes increased TNF-alpha production, leading to retinal ganglion cell death. Investigative Ophthalmology & Visual Science 2010, 51:6639-6651.
7. Benowitz L.I., Popovich P.G. Inflammation and axon regeneration. Current Opinion in Neurology 2011, 24:577-583.
8. Benowitz L., Yin Y. Rewiring the injured CNS: Lessons from the optic nerve. Experimental Neurology 2008, 209:389-398.
9. Berry M., Ahmed Z., Douglas M., Logan A. Epidermal growth factor receptor antagonists and CNS regeneration: Mechanisms and controversies. Brain Research Bulletin 2010, 84:289-299.
10. Berry M., Ahmed Z., Lorber B., Douglas M., Logan A. Regeneration of axons in the visual system. Restorative Neurology and Neuroscience 2008, 26:147-174.
11. Berry M., Barrett L., Seymour L., Baird A., Logan A. Gene therapy for central nervous system repair. Current Opinion in Molecular Therapeutics 2001, 3:338-349.
12. Berry M., Carlile J., Hunter A. Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. Journal of Neurocytology 1996, 25:147-170.
13. Berry M., Rees L., Hall S., Yiu P., Sievers J. Optic axons regenerate into sciatic nerve isografts only in the presence of Schwann cells. Brain Research Bulletin 1988, 20:223-231.
14. Bertrand J., Winton M.J., Rodriguez-Hernandez N., Campenot R.B., McKerracher L. Application of Rho antagonist to neuronal cell bodies promotes neurite growth in compartmented cultures and regeneration of retinal ganglion cell axons in the optic nerve of adult rats. The Journal of Neuroscience 2005, 25:1113-1121.
15. Bok D., Yasumura D., Matthes M.T., Ruiz A., Duncan J.L., Chappelow A.V., et al. Effects of adeno-associated virus-vectored ciliary neurotrophic factor on retinal structure and function in mice with a P216L rds/peripherin mutation. Experimental Eye Research 2002, 74:719-735.
16. Bray G., Aguayo A. Exploring the capacity of CNS neurons to survive injury, regrow axons and form new synapses in adult mammals. Neural regeneration and transplantation 1989, 67-78. Liss, New York. F. Seil (Ed.).
17. Caleo M., Menna E., Chierzi S., Cenni M.C., Maffei L. Brain-derived neurotrophic factor is an anterograde survival factor in the rat visual system. Current Biology 2000, 10:1155-1161.
18. Campbell G., Holt J.K., Shotton H.R., Anderson P.N., Bavetta S., Lieberman A.R. Spontaneous axonal regeneration after optic nerve injury in adult rat. Neuroreport 1999, 10:3955-3960.
19. Cao W., Li F., Steinberg R.H., Lavail M.M. Development of normal and injury-induced gene expression of aFGF, bFGF, CNTF, BDNF, GFAP and IGF-I in the rat retina. Experimental Eye Research 2001, 72:591-604.
20. Charalambous P., Hurst L.A., Thanos S. Engrafted chicken neural tube-derived stem cells support the innate propensity for axonal regeneration within the rat optic nerve. Investigative Ophthalmology & Visual Science 2008, 49:3513-3524.
21. Chen H., Weber A.J. Brain-derived neurotrophic factor reduces TrkB protein and mRNA in the normal retina and following optic nerve crush in adult rats. Brain Research 2004, 1011:99-106.
22. Cheng L., Sapieha P., Kittlerova P., Hauswirth W.W., Di Polo A. TrkB gene transfer protects retinal ganglion cells from axotomy-induced death in vivo. The Journal of Neuroscience 2002, 22:3977-3986.
23. Chierzi S., Fawcett J.W. Regeneration in the mammalian optic nerve. Restorative Neurology and Neuroscience 2001, 19:109-118.
24. Cho E.Y., So K.F. Sprouting of axon-like processes from axotomized retinal ganglion cells is influenced by the distance of axotomy from the cell body and the mode of transplantation of the peripheral nerve. Restorative Neurology and Neuroscience 1993, 6:29-34.
25. Chun M.H., Ju W.K., Kim K.Y., Lee M.Y., Hofmann H.D., Kirsch M., et al. Upregulation of ciliary neurotrophic factor in reactive Müller cells in the rat retina following optic nerve transection. Brain Research 2000, 868:358-362.
26. Cohen-Cory S., Lom B. Neurotrophic regulation of retinal ganglion cell synaptic connectivity: From axons and dendrites to synapses. The International Journal of Developmental Biology 2004, 48:947-956.
27. Cui Q., Cho K.S., So K.F., Yip H.K. Synergistic effect of Nogo-neutralizing antibody IN-1 and ciliary neurotrophic factor on axonal regeneration in adult rodent visual systems. Journal of Neurotrauma 2004, 21:617-625.
28. Cui Q., Harvey A.R. NT-4/5 reduces naturally occurring retinal ganglion cell death in neonatal rats. Neuroreport 1994, 5:1882-1884.
29. Cui Q., Harvey A. At least two mechanisms are involved in the death of retinal ganglion cells following target ablation in neonatal rats. The Journal of Neuroscience 1995, 15:8143-8155.
30. Cui Q., Tang L.S., Hu B., So K.F., Yip H.K. Expression of trkA, trkB, and trkC in injured and regenerating retinal ganglion cells of adult rats. Investigative Ophthalmology & Visual Science 2002, 43:1954-1964.
31. Cui Q., Yin Y., Benowitz L.I. The role of macrophages in optic nerve regeneration. Neuroscience 2009, 158:1039-1048.
32. Cui Q., Yip H.K., Zhao R.C.H., So K.-F., Harvey A.R. Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Molecular and Cellular Neuroscience 2003, 22:49-61.
33. Dallimore E.J., Cui Q., Beazley L.D., Harvey A.R. Postnatal innervation of the rat superior colliculus by axons of late-born retinal ganglion cells. The European Journal of Neuroscience 2002, 16:1295-1304.
34. Dallimore E.J., Park K.K., Pollett M.A., Taylor J.S., Harvey A.R. The life, death and regenerative ability of immature and mature rat retinal ganglion cells are influenced by their birthdate. Experimental Neurology 2010, 225:353-365.
35. Davies A.M. Regulation of neuronal survival and death by extracellular signals during development. The EMBO Journal 2003, 22:2537-2545.
36. de Araujo E.G., Linden R. Trophic factors produced by retinal cells increase the survival of retinal ganglion cells in vitro. The European Journal of Neuroscience 1993, 5:1181-1188.
37. de Winter F., Cui Q., Symons N., Verhaagen J., Harvey A.R. Expression of class-3 semaphorins and their receptors in the neonatal and adult rat retina. Investigative Ophthalmology & Visual Science 2004, 45:4554-4562.
38. Di Polo A., Aigner L.J., Dunn R.J., Bray G.M., Aguayo A.J. Prolonged delivery of brain-derived neurotrophic factor by adenovirus-infected Muller cells temporarily rescues injured retinal ganglion cells. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:3978-3983.
39. Doster S.K., Lozano A.M., Aguayo A.J., Willard M.B. Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron 1991, 6:635-647.
40. Du J.L., Poo M.M. Rapid BDNF-induced retrograde synaptic modification in a developing retinotectal system. Nature 2004, 429:878-883.
41. Emerich D.F., Thanos C.G. NT-501: An ophthalmic implant of polymer-encapsulated ciliary neurotrophic factor-producing cells. Current Opinion in Molecular Therapeutics 2008, 10:506-515.
42. Fischer D., Petkova V., Thanos S., Benowitz L.I. Switching mature retinal ganglion cells to a robust growth state in vivo: Gene expression and synergy with RhoA inactivation. The Journal of Neuroscience 2004, 24:8726-8740.
43. Fournier A.E., McKerracher L. Expression of specific tubulin isotypes increases during regeneration of injured CNS neurons, but not after the application of brain-derived neurotrophic factor (BDNF). The Journal of Neuroscience 1997, 17:4623-4632.
44. Frank R.N. Growth factors in age-related macular degeneration: Pathogenic and therapeutic implications. Ophthalmic Research 1997, 29:341-353.
45. Frost D.O. BDNF/trkB signaling in the developmental sculpting of visual connections. Progress in Brain Research 2001, 134:35-49.
46. Fu Q.L., Hu B., Li X., Shao Z., Shi J.B., Wu W., et al. LINGO-1 negatively regulates TrkB phosphorylation after ocular hypertension. The European Journal of Neuroscience 2010, 31:1091-1097.
47. Fu Q.L., Li X., Yip H.K., Shao Z., Wu W., Mi S., et al. Combined effect of brain-derived neurotrophic factor and LINGO-1 fusion protein on long-term survival of retinal ganglion cells in chronic glaucoma. Neuroscience 2009, 162:375-382.
48. Gao H., Qiao X., Hefti F., Hollyfield J.G., Knusel B. Elevated mRNA expression of brain-derived neurotrophic factor in retinal ganglion cell layer after optic nerve injury. Investigative Ophthalmology & Visual Science 1997, 38:1840-1847.
49. Gaub P., Joshi Y., Wuttke A., Naumann U., Schnichels S., Heiduschka P., et al. The histone acetyltransferase p300 promotes intrinsic axonal regeneration. Brain 2011, 134:2134-2148.
50. Goldberg J.L., Barres B.A. The relationship between neuronal survival and regeneration. Annual Review of Neuroscience 2000, 23:579.
51. Goldberg J.L., Klassen M.P., Hua Y., Barres B.A. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 2002, 296:1860-1864.
52. Harper M.M., Grozdanic S.D., Blits B., Kuehn M.H., Zamzow D., Buss J.E., et al. Transplantation of BDNF-secreting mesenchymal stem cells provides neuroprotection in chronically hypertensive rat eyes. Investigative Ophthalmology & Visual Science 2011, 52:4506-4515.
53. Harvey A.R., Hu Y., Leaver S.G., Mellough C.B., Park K., Verhaagen J., et al. Gene therapy and transplantation in CNS repair: The visual system. Progress in Retinal and Eye Research 2006, 25:449-489.
54. Harvey A.R., Tan M.M. Spontaneous regeneration of adult rat retinal ganglion cell axons in vivo. Neuroreport 1992, 3:239-242.
55. Heiduschka P., Thanos S. Restoration of the retinofugal pathway. Progress in Retinal and Eye Research 2000, 19:577-606.
56. Hellström M., Harvey A.R. Retinal ganglion cell gene therapy and visual system repair. Current Gene Therapy 2011, 11:116-131.
57. Hellström M., Muhling J., Ehlert E.M., Verhaagen J., Pollett M.A., Hu Y., et al. Negative impact of rAAV2 mediated expression of SOCS3 on the regeneration of adult retinal ganglion cell axons. Molecular and Cellular Neuroscience 2011, 46:507-515.
58. Hellström M., Pollett M.A., Harvey A.R. Post-injury delivery of rAAV2-CNTF combined with short-term pharmacotherapy is neuroprotective and promotes extensive axonal regeneration after optic nerve trauma. Journal of Neurotrauma 2011, 28:2475-2483.
59. Hellström M., Ruitenberg M.J., Pollett M.A., Ehlert E.M., Twisk J., Verhaagen J., et al. Cellular tropism and transduction properties of seven adeno-associated viral vector serotypes in adult retina after intravitreal injection. Gene Therapy 2009, 16:521-532.
60. Higuero A.M., Sanchez-Ruiloba L., Doglio L.E., Portillo F., Abad-Rodriguez J., Dotti C.G., et al. Kidins220/ARMS modulates the activity of microtubule-regulating proteins and controls neuronal polarity and development. The Journal of Biological Chemistry 2010, 285:1343-1357.
61. Hill A.J., Zwart I., Samaranayake A.N., Al-Allaf F., Girdlestone J., Mehmet H., et al. Rat neurosphere cells protect axotomized rat retinal ganglion cells and facilitate their regeneration. Journal of Neurotrauma 2009, 26:1147-1156.
62. Hirsch S., Bähr M. Immunocytochemical characterization of reactive optic nerve astrocytes and meningeal cells. Glia 1999, 26:36-46.
63. Hirsch S., Labes M., Bähr M. Changes in BDNF and neurotrophin receptor expression in degenerating and regenerating rat retinal ganglion cells. Restorative Neurology and Neuroscience 2000, 17:125-134.
64. Hu Y., Arulpragasam A., Plant G.W., Hendriks W.T., Cui Q., Harvey A.R. The importance of transgene and cell type on the regeneration of adult retinal ganglion cell axons within reconstituted bridging grafts. Experimental Neurology 2007, 207:314-328.
65. Hu Y., Cho S., Goldberg J.L. Neurotrophic effect of a novel TrkB agonist on retinal ganglion cells. Investigative Ophthalmology & Visual Science 2010, 51:1747-1754.
66. Hu Y., Cui Q., Harvey A.R. Interactive effects of C3, cyclic AMP and ciliary neurotrophic factor on adult retinal ganglion cell survival and axonal regeneration. Molecular and Cellular Neuroscience 2007, 34:88-98.
67. Hu Y., Leaver S.G., Plant G.W., Hendriks W.T., Niclou S.P., Verhaagen J., et al. Lentiviral-mediated transfer of CNTF to Schwann cells within reconstructed peripheral nerve grafts enhances adult retinal ganglion cell survival and axonal regeneration. Molecular Therapy 2005, 11:906-915.
68. Isenmann S., Klöcker N., Gravel C., Bähr M. Short communication: Protection of axotomized retinal ganglion cells by adenovirally delivered BDNF in vivo. The European Journal of Neuroscience 1998, 10:2751-2756.
69. Ishikawa H., Takano M., Matsumoto N., Sawada H., Ide C., Mimura O., et al. Effect of GDNF gene transfer into axotomized retinal ganglion cells using in vivo electroporation with a contact lens-type electrode. Gene Therapy 2005, 12:289-298.
70. Jo S.A., Wang E., Benowitz L.I. Ciliary neurotrophic factor is an axogenesis factor for retinal ganglion cells. Neuroscience 1999, 89:579-591.
71. Johnson E.C., Doser T.A., Cepurna W.O., Dyck J.A., Jia L., Guo Y., et al. Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma. Investigative Ophthalmology & Visual Science 2011, 52:504-518.
72. Ju W.K., Kim K.Y., Lee M.Y., Hofmann H.D., Kirsch M., Cha J.H., et al. Up-regulated CNTF plays a protective role for retrograde degeneration in the axotomized rat retina. Neuroreport 2000, 11:3893-3896.
73. Kaplan D.R., Miller F.D. Neurotrophin signal transduction in the nervous system. Current Opinion in Neurobiology 2000, 10:381-391.
74. Kermer P., Klocker N., Labes M., Bahr M. Insulin-like growth factor-I protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 In vivo. The Journal of Neuroscience 2000, 20:2-8.
75. Kern T.S., Barber A.J. Retinal ganglion cells in diabetes. The Journal of Physiology 2008, 586:4401-4408.
76. Klöcker N., Braunling F., Isenmann S., Bähr M. In vivo neurotrophic effects of GDNF on axotomized retinal ganglion cells. Neuroreport 1997, 8:3439-3442.
77. Klöcker N., Jung M., Stuermer C.A., Bähr M. BDNF increases the number of axotomized rat retinal ganglion cells expressing GAP-43, L1, and TAG-1 mRNA-A supportive role for nitric oxide?. Neurobiology of Disease 2001, 8:103-113.
78. Koeberle P.D., Ball A.K. Neurturin enhances the survival of axotomized retinal ganglion cells in vivo: Combined effects with glial cell line-derived neurotrophic factor and brain-derived neurotrophic factor. Neuroscience 2002, 110:555-567.
79. Kong H., Boulter J., Weber J.L., Lai C., Chao M.V. An evolutionarily conserved transmembrane protein that is a novel downstream target of neurotrophin and ephrin receptors. The Journal of Neuroscience 2001, 21:176-185.
80. Kreutz M.R., Weise J., Dieterich D.C., Kreutz M., Balczarek P., Bockers T.M., et al. Rearrangement of the retino-collicular projection after partial optic nerve crush in the adult rat. The European Journal of Neuroscience 2004, 19:247-257.
81. Kugler S., Klöcker N., Kermer P., Isenmann S., Bähr M. Transduction of axotomized retinal ganglion cells by adenoviral vector administration at the optic nerve stump: An in vivo model system for the inhibition of neuronal apoptotic cell death. Gene Therapy 1999, 6:1759-1767.
82. Kurimoto T., Yin Y., Omura K., Gilbert H.Y., Kim D., Cen L.P., et al. Long-distance axon regeneration in the mature optic nerve: Contributions of oncomodulin, cAMP, and pten gene deletion. The Journal of Neuroscience 2010, 30:15654-15663.
83. Lawrence J.M., Keegan D.J., Muir E.M., Coffey P.J., Rogers J.H., Wilby M.J., et al. Transplantation of Schwann cell line clones secreting GDNF or BDNF into the retinas of dystrophic Royal College of Surgeons rats. Investigative Ophthalmology & Visual Science 2004, 45:267-274.
84. Leaver S.G., Cui Q., Bernard O., Harvey A.R. Cooperative effects of bcl-2 and AAV-mediated expression of CNTF on retinal ganglion cell survival and axonal regeneration in adult transgenic mice. The European Journal of Neuroscience 2006, 24:3323-3332.
85. Leaver S.G., Cui Q., Plant G.W., Arulpragasam A., Hisheh S., Verhaagen J., et al. AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells. Gene Therapy 2006, 13:1328-1341.
86. Lebrun-Julien F., Bertrand M.J., De Backer O., Stellwagen D., Morales C.R., Di Polo A., et al. ProNGF induces TNFalpha-dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3817-3822.
87. Lebrun-Julien F., Duplan L., Pernet V., Osswald I., Sapieha P., Bourgeois P., et al. Excitotoxic death of retinal neurons in vivo occurs via a non-cell-autonomous mechanism. The Journal of Neuroscience 2009, 29:5536-5545.
88. Lebrun-Julien F., Morquette B., Douillette A., Saragovi H.U., Di Polo A. Inhibition of p75(NTR) in glia potentiates TrkA-mediated survival of injured retinal ganglion cells. Molecular and Cellular Neuroscience 2009, 40:410-420.
89. Leibinger M., Muller A., Andreadaki A., Hauk T.G., Kirsch M., Fischer D. Neuroprotective and axon growth-promoting effects following inflammatory stimulation on mature retinal ganglion cells in mice depend on ciliary neurotrophic factor and leukemia inhibitory factor. The Journal of Neuroscience 2009, 29:14334-14341.
90. Levkovitch-Verbin H., Sadan O., Vander S., Rosner M., Barhum Y., Melamed E., et al. Intravitreal injections of neurotrophic factors secreting mesenchymal stem cells are neuroprotective in rat eyes following optic nerve transection. Investigative Ophthalmology & Visual Science 2010, 51:6394-6400.
91. Li Z., Dong X., Wang Z., Liu W., Deng N., Ding Y., et al. Regulation of PTEN by Rho small GTPases. Nature Cell Biology 2005, 7:399-404.
92. Liang F.Q., Aleman T.S., Dejneka N.S., Dudus L., Fisher K.J., Maguire A.M., et al. Long-term protection of retinal structure but not function using rAAV. CNTF in animal models of retinitis pigmentosa. Molecular Therapy 2001, 4:461-472.
93. Lindqvist N., Peinado-Ramonn P., Vidal-Sanz M., Hallbook F. GDNF, Ret, GFRalpha1 and 2 in the adult rat retino-tectal system after optic nerve transection. Experimental Neurology 2004, 187:487-499.
94. Lingor P., Tönges L., Pieper N., Bermel C., Barski E., Planchamp V., et al. ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain 2008, 131:250-263.
95. Logan A., Ahmed Z., Baird A., Gonzalez A.M., Berry M. Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 2006, 129:490-502.
96. Loh N.K., Woerly S., Bunt S.M., Wilton S.D., Harvey A.R. The regrowth of axons within tissue defects in the CNS is promoted by implanted hydrogel matrices that contain BDNF and CNTF producing fibroblasts. Experimental Neurology 2001, 170:72-84.
97. Lund R.D., Ono S.J., Keegan D.J., Lawrence J.M. Retinal transplantation: Progress and problems in clinical application. Journal of Leukocyte Biology 2003, 74:151-160.
98. Ma Y.-T., Hsieh T., Forbes M.E., Johnson J.E., Frost D.O. BDNF injected into the superior colliculus reduces developmental retinal ganglion cell death. The Journal of Neuroscience 1998, 18:2097-2107.
99. Ma C., Taylor J. Trophic responsiveness of purified postnatal and adult rat retinal ganglion cells. Cell and Tissue Research 2010, 339:297-310.
100. Maffei L., Carmignoto G., Perry V.H., Candeo P., Ferrari G. Schwann cells promote the survival of rat retinal ganglion cells after optic nerve section. Proceedings of the National Academy of Sciences of the United States of America 1990, 87:1855-1859.
101. Mansour-Robaey S., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:1632-1636.
102. Marler K.J., Poopalasundaram S., Broom E.R., Wentzel C., Drescher U. Pro-neurotrophins secreted from retinal ganglion cell axons are necessary for ephrinA-p75NTR-mediated axon guidance. Neural Development 2010, 5:30.
103. Marotte L.R., Vidovic M., Wheeler E., Jhaveri S. Brain-derived neurotrophic factor is expressed in a gradient in the superior colliculus during development of the retinocollicular projection. The European Journal of Neuroscience 2004, 20:843-847.
104. McKerracher L., Winton M.J. Nogo on the go. Neuron 2002, 36:345-348.
105. Mey J., Thanos S. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Research 1993, 602:304-317.
106. Meyer-Franke A., Kaplan M.R., Pfieger F.W., Barres B.A. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 1995, 15:805-819.
107. Meyer-Franke A., Wilkinson G.A., Kruttgen A., Hu M., Munro E., Hanson M.G., et al. Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 1998, 21:681-693.
108. Mo X., Yokoyama A., Oshitari T., Negishi H., Dezawa M., Mizota A., et al. Rescue of axotomized retinal ganglion cells by BDNF gene electroporation in adult rats. Investigative Ophthalmology & Visual Science 2002, 43:2401-2405.
109. Moore D.L., Apara A., Goldberg J.L. Krüppel-like transcription factors in the nervous system: Novel players in neurite outgrowth and axon regeneration. Molecular and Cellular Neuroscience 2011, 47:233-243.
110. Muller A., Hauk T.G., Fischer D. Astrocyte-derived CNTF switches mature RGCs to a regenerative state following inflammatory stimulation. Brain 2007, 130:3308-3320.
111. Park K.K., Hu Y., Muhling J., Pollett M.A., Dallimore E.J., Turnley A.M., et al. Cytokine-induced SOCS expression is inhibited by cAMP analogue: Impact on regeneration in injured retina. Molecular and Cellular Neuroscience 2009, 41:313-324.
112. Park K.K., Liu K., Hu Y., Kanter J.L., He Z. PTEN/mTOR and axon regeneration. Experimental Neurology 2010, 223:45-50.
113. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
114. Park K., Luo J.M., Hisheh S., Harvey A.R., Cui Q. Cellular mechanisms associated with spontaneous and ciliary neurotrophic factor-cAMP-induced survival and axonal regeneration of adult retinal ganglion cells. The Journal of Neuroscience 2004, 24:10806-10815.
115. Pease M.E., McKinnon S.J., Quigley H.A., Kerrigan-Baumrind L.A., Zack D.J. Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Investigative Ophthalmology & Visual Science 2000, 41:764-774.
116. Pease M.E., Zack D.J., Berlinicke C., Bloom K., Cone F., Wang Y., et al. Effect of CNTF on retinal ganglion cell survival in experimental glaucoma. Investigative Ophthalmology & Visual Science 2009, 50:2194-2200.
117. Peinado-Ramon P., Salvador M., Villegas-Pérez M.P., Vidal-Sanz M. Effects of axotomy and intraocular administration of NT-4, NT-3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells. A quantitative in vivo study. Investigative Ophthalmology & Visual Science 1996, 37:489-500.
118. Perez M.T., Caminos E. Expression of brain-derived neurotrophic factor and of its functional receptor in neonatal and adult rat retina. Neuroscience Letters 1995, 183:96-99.
119. Pernet V., Di Polo A. Synergistic action of brain-derived neurotrophic factor and lens injury promotes retinal ganglion cell survival, but leads to optic nerve dystrophy in vivo. Brain 2006, 129:1014-1026.
120. Petratos S., Ozturk E., Azari M.F., Kenny R., Young Lee J., Magee K.A., et al. Limiting multiple sclerosis related axonopathy by blocking Nogo receptor and CRMP-2 phosphorylation. Brain 2012, 135:1794-1818.
121. Plant G.W., Harvey A.R., Chirila T.V. Axonal growth within poly (2-hydroxyethyl methacrylate) sponges infiltrated with Schwann cells and implanted into the lesioned rat optic tract. Brain Research 1995, 671:119-130.
122. Plant G.W., Woerly S., Harvey A.R. Hydrogels containing peptide or aminosugar sequences implanted into the rat brain: Influence on cellular migration and axonal growth. Experimental Neurology 1997, 143:287-299.
123. Pollock G.S., Robichon R., Boyd K.A., Kerkel K.A., Kramer M., Lyles J., et al. TrkB receptor signaling regulates developmental death dynamics, but not final number, of retinal ganglion cells. The Journal of Neuroscience 2003, 23:10137-10145.
124. Poopalasundaram S., Marler K.J., Drescher U. EphrinA6 on chick retinal axons is a key component for p75(NTR)-dependent axon repulsion and TrkB-dependent axon branching. Molecular and Cellular Neuroscience 2011, 47:131-136.
125. Read S.P., Cashman S.M., Kumar-Singh R. POD nanoparticles expressing GDNF provide structural and functional rescue of light-induced retinal degeneration in an adult mouse. Molecular Therapy 2010, 18:1917-1926.
126. Rickman D.W., Brecha N.C. Expression of the proto-oncogene, trk, receptors in the developing rat retina. Visual Neuroscience 1995, 12:215-222.
127. Robinson M., Adu J., Davies A.M. Timing and regulation of trkB and BDNF mRNA expression in placode-derived sensory neurons and their targets. The European Journal of Neuroscience 1996, 8:2399-2406.
128. Rodger J., Drummond E.S., Hellstrom M., Robertson D., Harvey A.R. Long-term gene therapy causes transgene-specific changes in the morphology of regenerating retinal ganglion cells. PLoS One 2012, 7:e31061.
129. Rodger J., Goto H., Cui Q., Chen P.B., Harvey A.R. cAMP regulates axon outgrowth and guidance during optic nerve regeneration in goldfish. Molecular and Cellular Neuroscience 2005, 30:452-464.
130. Rodriguez-Tebar A., Jeffrey P.L., Thoenen H., Barde Y.-A. The survival of chick retinal ganglion cells in response to brain-derived neurotrophic factor depends on their embryonic age. Developmental Biology 1989, 136:296-303.
131. Rohrer B., LaVail M.M., Jones K.R., Reichardt L.F. Neurotrophin receptor TrkB activation is not required for the postnatal survival of retinal ganglion cells in vivo. Experimental Neurology 2001, 172:81-91.
132. Ruitenberg M.J., Blits B., Dijkhuizen P.A., te Beek E.T., Bakker A., van Heerikhuize J.J., et al. 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. Neurobiology of Disease 2004, 15:394-406.
133. Sapieha P.S., Peltier M., Rendahl K.G., Manning W.C., Di Polo A. Fibroblast growth factor-2 gene delivery stimulates axon growth by adult retinal ganglion cells after acute optic nerve injury. Molecular and Cellular Neuroscience 2003, 24:656-672.
134. Sarup V., Patil K., Sharma S.C. Ciliary neurotrophic factor and its receptors are differentially expressed in the optic nerve transected adult rat retina. Brain Research 2004, 1013:152-158.
135. Sauvé Y., Sawai H., Rasminsky M. Functional synaptic connections made by regenerated retinal ganglion cell axons in the superior colliculus of adult hamsters. The Journal of Neuroscience 1995, 15:665-675.
136. Sawai H., Clarke D.B., Kittlerova P., Bray G.M., Aguayo A.J. Brain-derived neurotrophic factor and neurotrophin-4/5 stimulate growth of axonal branches from regenerating retinal ganglion cells. The Journal of Neuroscience 1996, 16:3887-3894.
137. Schlichtenbrede F.C., MacNeil A., Bainbridge J.W., Tschernutter M., Thrasher A.J., Smith A.J., et al. Intraocular gene delivery of ciliary neurotrophic factor results in significant loss of retinal function in normal mice and in the Prph2Rd2/Rd2 model of retinal degeneration. Gene Therapy 2003, 10:523-527.
138. Schmeer C., Straten G., Kügler S., Gravel C., Bähr M., Isenmann S. Dose-dependent rescue of axotomized rat retinal ganglion cells by adenovirus-mediated expression of glial cell-line derived neurotrophic factor in vivo. The European Journal of Neuroscience 2002, 15:637-643.
139. Schuettauf F., Vorwerk C., Naskar R., Orlin A., Quinto K., Zurakowski D., et al. Adeno-associated viruses containing bFGF or BDNF are neuroprotective against excitotoxicity. Current Eye Research 2004, 29:379-386.
140. Seki M., Nawa H., Fukuchi T., Abe H., Takei N. BDNF is upregulated by postnatal development and visual experience: Quantitative and immunohistochemical analyses of BDNF in the rat retina. Investigative Ophthalmology & Visual Science 2003, 44:3211-3218.
141. Shen S., Wiemelt A.P., McMorris F.A., Barres B.A. Retinal ganglion cells lose trophic responsiveness after axotomy. Neuron 1999, 23:285-295.
142. Sieving P.A., Caruso R.C., Tao W., Coleman H.R., Thompson D.J., Fullmer K.R., et al. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: Phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:3896-3901.
143. Smith P.D., Sun F., Park K.K., Cai B., Wang C., Kuwako K., et al. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 2009, 64:617-623.
144. Sommerfeld M.T., Schweigreiter R., Barde Y.-A., Hoppe E. Down-regulation of the neurotrophin receptor TrkB following ligand binding. The Journal of Biological Chemistry 2000, 275:8982-8990.
145. Spalding K.L., Cui Q., Harvey A.R. The effects of central administration of neurotrophins or transplants of fetal tectal tissue on retinal ganglion cell survival following removal of the superior colliculus in neonatal rats. Developmental Brain Research 1998, 107:133-142.
146. Spalding K.L., Rush R.A., Harvey A.R. Target-derived and locally derived neurotrophins support retinal ganglion cell survival in the neonatal rat retina. Journal of Neurobiology 2004, 60:319-327.
147. Straten G., Schmeer C., Kretz A., Gerhardt E., Kugler S., Schulz J.B., et al. Potential synergistic protection of retinal ganglion cells from axotomy-induced apoptosis by adenoviral administration of glial cell line-derived neurotrophic factor and X-chromosome-linked inhibitor of apoptosis. Neurobiology of Disease 2002, 11:123-133.
148. Sun F., He Z. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Current Opinion in Neurobiology 2010, 20:510-518.
149. Thanos S. Adult retinofugal axons regenerating through peripheral nerve grafts can restore the light-induced pupilloconstriction reflex. The European Journal of Neuroscience 1992, 4:691-699.
150. Tonges L., Koch J.C., Bähr M., Lingor P. ROCKing regeneration: Rho kinase inhibition as molecular target for neurorestoration. Frontiers in Molecular Neuroscience 2011, 4:39.
151. Tonges L., Ostendorf T., Lamballe F., Genestine M., Dono R., Koch J.C., et al. Hepatocyte growth factor protects retinal ganglion cells by increasing neuronal survival and axonal regeneration in vitro and in vivo. Journal of Neurochemistry 2011, 117:892-903.
152. Trakhtenberg E.F., Goldberg J.L. Epigenetic regulation of axon and dendrite growth. Frontiers in Molecular Neuroscience 2012, 5:24.
153. Tropea D., Caleo M., Maffei L. Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. The Journal of Neuroscience 2003, 23:7034-7044.
154. Ugolini G., Cremisi F., Maffei L. TrkA, TrkB and p75 mRNA expression is developmentally regulated in the rat retina. Brain Research 1995, 704:121-124.
155. Valter K., Bisti S., Gargini C., Di Loreto S., Maccarone R., Cervetto L., et al. Time course of neurotrophic factor upregulation and retinal protection against light-induced damage after optic nerve section. Investigative Ophthalmology & Visual Science 2005, 46:1748-1754.
156. van Adel B.A., Arnold J.M., Phipps J., Doering L.C., Ball A.K. Ciliary neurotrophic factor protects retinal ganglion cells from axotomy-induced apoptosis via modulation of retinal glia in vivo. Journal of Neurobiology 2005, 63:215-234.
157. Vanselow J., Dutting D., Thanos S. Target dependence of chick retinal ganglion cells during embryogenesis: Cell survival and dendritic development. The Journal of Comparative Neurology 1990, 295:235-247.
158. Vecino E., Garcia-Crespo D., Garcia M., Martinez-Millan L., Sharma S.C., Carrascal E. Rat retinal ganglion cells co-express brain derived neurotrophic factor (BDNF) and its receptor TrkB. Vision Research 2002, 42:151-157.
159. Vidal-Sanz M., Aviles-Trigueros M., Whiteley S.J., Sauvé Y., Lund R.D. Reinnervation of the pretectum in adult rats by regenerated retinal ganglion cell axons: Anatomical and functional studies. Progress in Brain Research 2002, 137:443-452.
160. Vukovic J., Plant G.W., Ruitenberg M.J., Harvey A.R. 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 Biology 2007, 3:105-117.
161. Wadhwa S., Paliwal R., Paliwal S.R., Vyas S.P. Nanocarriers in ocular drug delivery: An update review. Current Pharmaceutical Design 2009, 15:2724-2750.
162. Watanabe M. Regeneration of optic nerve fibers of adult mammals. Development, Growth & Differentiation 2010, 52:567-576.
163. Weber A.J., Viswanathan S., Ramanathan C., Harman C.D. Combined application of BDNF to the eye and brain enhances ganglion cell survival and function in the cat after optic nerve injury. Investigative Ophthalmology & Visual Science 2010, 51:327-334.
164. Weise J., Isenmann S., Klöcker N., Kugler S., Hirsch S., Gravel C., et al. Adenovirus-mediated expression of ciliary neurotrophic factor (CNTF) rescues axotomized rat retinal ganglion cells but does not support axonal regeneration in vivo. Neurobiology of Disease 2000, 7:212-223.
165. Wen R., Tao W., Li Y., Sieving P.A. CNTF and retina. Progress in Retinal and Eye Research 2012, 31:136-151.
166. Wordinger R.J., Lambert W., Agarwal R., Liu X., Clark A.F. Cells of the human optic nerve head express glial cell line-derived neurotrophic factor (GDNF) and the GDNF receptor complex. Molecular Vision 2003, 9:249-256.
167. Wu W.C., Lai C.C., Chen S.L., Sun M.H., Xiao X., Chen T.L., et al. GDNF gene therapy attenuates retinal ischemic injuries in rats. Molecular Vision 2004, 10:93-102.
168. Yan Q., Wang J., Matheson C.R., Urich J.L. Glial cell line-derived neurotrophic factor (GDNF) promotes the survival of axotomized retinal ganglion cells in adult rats: Comparison to and combination with brain-derived neurotrophic factor (BDNF). Journal of Neurobiology 1999, 38:382-390.
169. Yin Y., Cui Q., Li Y., Irwin N., Fischer D., Harvey A.R., et al. Macrophage-derived factors stimulate optic nerve regeneration. The Journal of Neuroscience 2003, 23:2284-2293.
170. Yoneda A., Morgan-Fisher M., Wait R., Couchman J.R., Wewer U.M. A collapsin response mediator protein 2 isoform controls myosin II-mediated cell migration and matrix assembly by trapping ROCK II. Molecular and Cellular Biology 2012, 32:1788-1804.
171. Zanin M.P., Pettingill L.N., Harvey A.R., Emerich D.F., Thanos C.G., Shepherd R.K. The development of encapsulated cell technologies as therapies for neurological and sensory diseases. Journal of Controlled Release 2012, 160:3-13.
172. Zhang C.W., Lu Q., You S.W., Zhi Y., Yip H.K., Wu W., et al. CNTF and BDNF have similar effects on retinal ganglion cell survival but differential effects on nitric oxide synthase expression soon after optic nerve injury. Investigative Ophthalmology & Visual Science 2005, 46:1497-1503.
173. Zhi Y., Lu Q., Zhang C.W., Yip H.K., So K.F., Cui Q. Different optic nerve injury sites result in different responses of retinal ganglion cells to brain-derived neurotrophic factor but not neurotrophin-4/5. Brain Research 2005, 1047:224-232.
174. Zwart I., Hill A.J., Al-Allaf F., Shah M., Girdlestone J., Sanusi A.B., et al. Umbilical cord blood mesenchymal stromal cells are neuroprotective and promote regeneration in a rat optic tract model. Experimental Neurology 2009, 216:439-448.