Promoting optic nerve regeneration

Progress in Retinal and Eye Research

Volumn 31, Issue 6, 2012, Pages 688-701

  Fischer, Dietmar ^a   Leibinger, Marco ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

CNTF; Inflammatory stimulation; Lens injury; LIF; Optic nerve regeneration; Taxol

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CYTOKINE; LEUKEMIA INHIBITORY FACTOR; MYELIN;

APOPTOSIS; CELL DEATH; DOWNSTREAM PROCESSING; GLIA; HUMAN; LENS DISEASE; NERVE CELL; NERVE FIBER; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; RETINA GANGLION CELL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL SURVIVAL; HUMANS; NERVE REGENERATION; OPTIC NERVE; OPTIC NERVE INJURIES; RETINAL GANGLION CELLS;

EID: 84867395898     PISSN: 13509462     EISSN: 18731635     Source Type: Journal    
DOI: 10.1016/j.preteyeres.2012.06.005     Document Type: Review

References (173)

1. Aguayo A.J., David S., Bray G.M. Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. J. Exp. Biol. 1981, 95:231-240.
2. Aguayo A.J., Vidal-Sanz M., Villegas-Perez M.P., Bray G.M. Growth and connectivity of axotomized retinal neurons in adult rats with optic nerves substituted by PNS grafts linking the eye and the midbrain. Ann. N. Y. Acad. Sci. 1987, 495:1-9.
3. Ahmed Z., Berry M., Logan A. ROCK inhibition promotes adult retinal ganglion cell neurite outgrowth only in the presence of growth promoting factors. Mol. Cell. Neurosci. 2009, 42:128-133.
4. Ahmed Z., Kalinski H., Berry M., Almasieh M., Ashush H., Slager N., Brafman A., Spivak I., Prasad N., Mett I., Shalom E., Alpert E., Di Polo A., Feinstein E., Logan A. Ocular neuroprotection by siRNA targeting caspase-2. Cell Death Dis. 2011, 2:e173.
5. Almasieh M., Wilson A.M., Morquette B., Cueva Vargas J.L., Di Polo A. The molecular basis of retinal ganglion cell death in glaucoma. Prog. Retin. Eye Res. 2012, 31:152-181.
6. Atwal J.K., Pinkston-Gosse J., Syken J., Stawicki S., Wu Y., Shatz C., Tessier-Lavigne M. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322:967-970.
7. Bahr M., Vanselow J., Thanos S. Ability of adult rat ganglion cells to regrow axons in vitro can be influenced by fibroblast growth factor and gangliosides. Neurosci. Lett. 1989, 96:197-201.
8. Becker T., Anliker B., Becker C.G., Taylor J., Schachner M., Meyer R.L., Bartsch U. Tenascin-R inhibits regrowth of optic fibers in vitro and persists in the optic nerve of mice after injury. Glia 2000, 29:330-346.
9. Benson M.D., Romero M.I., Lush M.E., Lu Q.R., Henkemeyer M., Parada L.F. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10694-10699.
10. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 1994, 14:4368-4374.
11. 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. J. Neurocytol. 1996, 25:147-170.
12. Berry M., Ahmed Z., Lorber B., Douglas M., Logan A. Regeneration of axons in the visual system. Restor. Neurol. Neurosci. 2008, 26:147-174.
13. 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. J. Neurosci. 2005, 25:1113-1121.
14. Bonilla I.E., Tanabe K., Strittmatter S.M. Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J. Neurosci. 2002, 22:1303-1315.
15. Bray G.M., Villegas-Perez M.P., Vidal-Sanz M., Aguayo A.J. The use of peripheral nerve grafts to enhance neuronal survival, promote growth and permit terminal reconnections in the central nervous system of adult rats. J. Exp. Biol. 1987, 132:5-19.
16. Buckingham B.P., Inman D.M., Lambert W., Oglesby E., Calkins D.J., Steele M.R., Vetter M.L., Marsh-Armstrong N., Horner P.J. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J. Neurosci. 2008, 28:2735-2744.
17. Cai X., Yuan R., Hu Z., Chen C., Yu J., Zheng Z., Ye J. Expression of PirB protein in intact and injured optic nerve and retina of mice. Neurochem. Res. 2012, 37:647-654.
18. Cajal Ry Degeneration and Regeneration of the Nervous System 1991, Oxford UP, New York.
19. Cellerino A., Bahr M., Isenmann S. Apoptosis in the developing visual system. Cell Tissue Res. 2000, 301:53-69.
20. Chaudhary P., Ahmed F., Quebada P., Sharma S.C. Caspase inhibitors block the retinal ganglion cell death following optic nerve transection. Brain Res. Mol. Brain Res. 1999, 67:36-45.
21. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ F., Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000, 403:434-439.
22. Chen C., Chen X., Yin X., Yuan R., Wang B., Ye J. NgR RNA interference, combined with zymosan intravitreal injection, enhances optic nerve regeneration. J. Neurochem. 2009, 110:1628-1634.
23. Cheung Z.H., Chan Y.M., Siu F.K., Yip H.K., Wu W., Leung M.C., So K.F. Regulation of caspase activation in axotomized retinal ganglion cells. Mol. Cell. Neurosci. 2004, 25:383-393.
24. Chierzi S., Fawcett J.W. Regeneration in the mammalian optic nerve. Restor. Neurol. Neurosci. 2001, 19:109-118.
25. Chierzi S., Strettoi E., Cenni M.C., Maffei L. Optic nerve crush: axonal responses in wild-type and bcl-2 transgenic mice. J. Neurosci. 1999, 19:8367-8376.
26. Cohen A., Bray G.M., Aguayo A.J. Neurotrophin-4/5 (NT-4/5) increases adult rat retinal ganglion cell survival and neurite outgrowth in vitro. J. Neurobiol. 1994, 25:953-959.
27. Compston A. Mechanisms of axon-glial injury of the optic nerve. Eye (Lond) 2004, 18:1182-1187.
28. Conde C., Caceres A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 2009, 10:319-332.
29. Cui Q., Lu Q., So K.F., Yip H.K. CNTF, not other trophic factors, promotes axonal regeneration of axotomized retinal ganglion cells in adult hamsters. Invest. Ophthalmol. Vis. Sci. 1999, 40:760-766.
30. Cui Q., Yip H.K., Zhao R.C., So K.F., Harvey A.R. Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol. Cell. Neurosci. 2003, 22:49-61.
31. de Lima S., Koriyama Y., Kurimoto T., Oliveira J.T., Yin Y., Li Y., Gilbert H.Y., Fagiolini M., Martinez A.M., Benowitz L. Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:9149-9154.
32. Derry W.B., Wilson L., Jordan M.A. Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry 1995, 34:2203-2211.
33. Derry W.B., Wilson L., Khan I.A., Luduena R.F., Jordan M.A. Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified beta-tubulin isotypes. Biochemistry 1997, 36:3554-3562.
34. 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. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:3978-3983.
35. Dickendesher T.L., Baldwin K.T., Mironova Y.A., Koriyama Y., Raiker S.J., Askew K.L., Wood A., Geoffroy C.G., Zheng B., Liepmann C.D., Katagiri Y., Benowitz L.I., Geller H.M., Giger R.J. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat. Neurosci. 2012, 15:703-712.
36. Domeniconi M., Cao Z., Spencer T., Sivasankaran R., Wang K., Nikulina E., Kimura N., Cai H., Deng K., Gao Y., He Z., Filbin M. Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 2002, 35:283-290.
37. Duffy P., Wang X., Siegel C.S., Tu N., Henkemeyer M., Cafferty W.B., Strittmatter S.M. Myelin-derived ephrinB3 restricts axonal regeneration and recovery after adult CNS injury. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:5063-5068.
38. Ebadi M., Bashir R.M., Heidrick M.L., Hamada F.M., Refaey H.E., Hamed A., Helal G., Baxi M.D., Cerutis D.R., Lassi N.K. Neurotrophins and their receptors in nerve injury and repair. Neurochem. Int. 1997, 30:347-374.
39. Ellezam B., Selles-Navarro I., Manitt C., Kennedy T.E., McKerracher L. Expression of netrin-1 and its receptors DCC and UNC-5H2 after axotomy and during regeneration of adult rat retinal ganglion cells. Exp. Neurol. 2001, 168:105-115.
40. Ernst M., Jenkins B.J. Acquiring signalling specificity from the cytokine receptor gp130. Trends Genet.: TIG 2004, 20:23-32.
41. Fischer D. What are the principal mediators of optic nerve regeneration after inflammatory stimulation in the eye?. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:E8.
42. Fischer D. Stimulating axonal regeneration of mature retinal ganglion cells and overcoming inhibitory signaling. Cell Tissue Res. 2012.
43. Fischer D., Pavlidis M., Thanos S. Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Invest. Ophthalmol. Vis. Sci. 2000, 41:3943-3954.
44. Fischer D., Heiduschka P., Thanos S. Lens-injury-stimulated axonal regeneration throughout the optic pathway of adult rats. Exp. Neurol. 2001, 172:257-272.
45. Fischer D., He Z., Benowitz L.I. Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J. Neurosci. 2004, 24:1646-1651.
46. 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. J. Neurosci. 2004, 24:8726-8740.
47. Fischer D., Hauk T.G., Müller A., Thanos S. Crystallins of the beta/gamma-superfamily mimic the effects of lens injury and promote axon regeneration. Mol. Cell. Neurosci. 2008, 37:471-479.
48. Fournier A.E., GrandPre T., Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409:341-346.
49. Fu S.Y., Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 1997, 14:67-116.
50. Fukada T., Hibi M., Yamanaka Y., Takahashi-Tezuka M., Fujitani Y., Yamaguchi T., Nakajima K., Hirano T. Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis. Immunity 1996, 5:449-460.
51. Geraldo S., Gordon-Weeks P.R. Cytoskeletal dynamics in growth-cone steering. J. Cell Sci. 2009, 122:3595-3604.
52. Goldberg J.L., Espinosa J.S., Xu Y., Davidson N., Kovacs G.T., Barres B.A. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 2002, 33:689-702.
53. 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.
54. Goldberg J.L., Vargas M.E., Wang J.T., Mandemakers W., Oster S.F., Sretavan D.W., Barres B.A. An oligodendrocyte lineage-specific semaphorin, Sema5A, inhibits axon growth by retinal ganglion cells. J. Neurosci. 2004, 24:4989-4999.
55. GrandPre T., Nakamura F., Vartanian T., Strittmatter S.M. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 2000, 403:439-444.
56. Grosskreutz C.L., Hanninen V.A., Pantcheva M.B., Huang W., Poulin N.R., Dobberfuhl A.P. FK506 blocks activation of the intrinsic caspase cascade after optic nerve crush. Exp. Eye Res. 2005, 80:681-686.
57. Grozdanov V., Müller A., Sengottuvel V., Leibinger M., Fischer D. A method for preparing primary retinal cell cultures for evaluating the neuroprotective and neuritogenic effect of factors on axotomized mature CNS neurons. Curr. Protoc. Neurosci. 2010, (Chapter 3:Unit 3 22).
58. Gutman C.R., Strittmatter W.J., Weisgraber K.H., Matthew W.D. Apolipoprotein E binds to and potentiates the biological activity of ciliary neurotrophic factor. J. Neurosci. 1997, 17:6114-6121.
59. Hagino S., Iseki K., Mori T., Zhang Y., Hikake T., Yokoya S., Takeuchi M., Hasimoto H., Kikuchi S., Wanaka A. Slit and glypican-1 mRNAs are coexpressed in the reactive astrocytes of the injured adult brain. Glia 2003, 42:130-138.
60. Hauk T.G., Müller A., Lee J., Schwendener R., Fischer D. Neuroprotective and axon growth promoting effects of intraocular inflammation do not depend on oncomodulin or the presence of large numbers of activated macrophages. Exp. Neurol. 2008, 209:469-482.
61. Hauk T.G., Leibinger M., Müller A., Andreadaki N., Knippschild U., Fischer D. Intravitreal application of the Toll-like receptor 2 agonist Pam3Cys stimulates axon regeneration in the mature optic nerve. Invest. Ophthalmol. Vis. Sci. 2009.
62. Heinrich P.C., Behrmann I., Muller-Newen G., Schaper F., Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 1998, 334(2):297-314.
63. Heinrich P.C., Behrmann I., Haan S., Hermanns H.M., Muller-Newen G., Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 2003, 374:1-20.
64. Hellal F., Hurtado A., Ruschel J., Flynn K.C., Laskowski C.J., Umlauf M., Kapitein L.C., Strikis D., Lemmon V., Bixby J., Hoogenraad C.C., Bradke F. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 2011, 331:928-931.
65. Hellstrom M., Harvey A.R. Retinal ganglion cell gene therapy and visual system repair. Curr. Gene Ther. 2011, 11:116-131.
66. Hellstrom M., Muhling J., Ehlert E.M., Verhaagen J., Pollett M.A., Hu Y., Harvey A.R. Negative impact of rAAV2 mediated expression of SOCS3 on the regeneration of adult retinal ganglion cell axons. Mol. Cell. Neurosci. 2011, 46:507-515.
67. Hellstrom 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. J. Neurotrauma 2011.
68. Hemmann U., Gerhartz C., Heesel B., Sasse J., Kurapkat G., Grotzinger J., Wollmer A., Zhong Z., Darnell J.E., Graeve L., Heinrich P.C., Horn F. Differential activation of acute phase response factor/Stat3 and Stat1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130. II. Src homology SH2 domains define the specificity of stat factor activation. J. Biol. Chem. 1996, 271:12999-13007.
69. Hsieh S.H., Ferraro G.B., Fournier A.E. Myelin-associated inhibitors regulate cofilin phosphorylation and neuronal inhibition through LIM kinase and Slingshot phosphatase. J. Neurosci. 2006, 26:1006-1015.
70. Inoue T., Hosokawa M., Morigiwa K., Ohashi Y., Fukuda Y. Bcl-2 overexpression does not enhance in vivo axonal regeneration of retinal ganglion cells after peripheral nerve transplantation in adult mice. J. Neurosci. 2002, 22:4468-4477.
71. Ji B., Li M., Wu W.T., Yick L.W., Lee X., Shao Z., Wang J., So K.F., McCoy J.M., Pepinsky R.B., Mi S., Relton J.K. LINGO-1 antagonist promotes functional recovery and axonal sprouting after spinal cord injury. Mol. Cell Neurosci. 2006, 33:311-320.
72. Jo S.A., Wang E., Benowitz L.I. Ciliary neurotrophic factor is an axogenesis factor for retinal ganglion cells. Neuroscience 1999, 89:579-591.
73. Jo D., Liu D., Yao S., Collins R.D., Hawiger J. Intracellular protein therapy with SOCS3 inhibits inflammation and apoptosis. Nat. Med. 2005, 11:892-898.
74. Kaneko S., Iwanami A., Nakamura M., Kishino A., Kikuchi K., Shibata S., Okano H.J., Ikegami T., Moriya A., Konishi O., Nakayama C., Kumagai K., Kimura T., Sato Y., Goshima Y., Taniguchi M., Ito M., He Z., Toyama Y., Okano H. A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat. Med. 2006, 12:1380-1389.
75. Keirstead S.A., Rasminsky M., Fukuda Y., Carter D.A., Aguayo A.J., Vidal-Sanz M. Electrophysiologic responses in hamster superior colliculus evoked by regenerating retinal axons. Science 1989, 246:255-257.
76. Kermer P., Klocker N., Labes M., Thomsen S., Srinivasan A., Bahr M. Activation of caspase-3 in axotomized rat retinal ganglion cells in vivo. FEBS Lett. 1999, 453:361-364.
77. Kim H., Baumann H. Dual signaling role of the protein tyrosine phosphatase SHP-2 in regulating expression of acute-phase plasma proteins by interleukin-6 cytokine receptors in hepatic cells. Mol. Cell. Biol. 1999, 19:5326-5338.
78. Kischkel F.C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P.H., Peter M.E. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 1995, 14:5579-5588.
79. Kischkel F.C., Lawrence D.A., Chuntharapai A., Schow P., Kim K.J., Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 2000, 12:611-620.
80. Koeberle P.D., Ball A.K. Effects of GDNF on retinal ganglion cell survival following axotomy. Vis. Res. 1998, 38:1505-1515.
81. 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.
82. Kottis V., Thibault P., Mikol D., Xiao Z.C., Zhang R., Dergham P., Braun P.E. Oligodendrocyte-myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. J. Neurochem. 2002, 82:1566-1569.
83. Kurimoto T., Yin Y., Omura K., Gilbert H.Y., Kim D., Cen L.P., Moko L., Kugler S., Benowitz L.I. Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J. Neurosci. 2011, 30:15654-15663.
84. Lagord C., Berry M., Logan A. Expression of TGFbeta2 but not TGFbeta1 correlates with the deposition of scar tissue in the lesioned spinal cord. Mol. Cell. Neurosci. 2002, 20:69-92.
85. Lauren J., Airaksinen M.S., Saarma M., Timmusk T. Two novel mammalian Nogo receptor homologs differentially expressed in the central and peripheral nervous systems. Mol. Cell. Neurosci. 2003, 24:581-594.
86. 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. Eur. J. Neurosci. 2006, 24:3323-3332.
87. Leaver S.G., Cui Q., Plant G.W., Arulpragasam A., Hisheh S., Verhaagen J., Harvey A.R. AAV-mediated expression of CNTF promotes long-term survival and regeneration of adult rat retinal ganglion cells. Gene Ther. 2006, 13:1328-1341.
88. Lehmann M., Fournier A., Selles-Navarro I., Dergham P., Sebok A., Leclerc N., Tigyi G., McKerracher L. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J. Neurosci. 1999, 19:7537-7547.
89. Lehmann U., Schmitz J., Weissenbach M., Sobota R.M., Hortner M., Friederichs K., Behrmann I., Tsiaris W., Sasaki A., Schneider-Mergener J., Yoshimura A., Neel B.G., Heinrich P.C., Schaper F. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Biol. Chem. 2003, 278:661-671.
90. Leibinger M., Müller 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. J. Neurosci. 2009, 29:14334-14341.
91. Leibinger M., Andreadaki A., Fischer D. Role of mTOR in neuroprotection and axon regeneration after inflammatory stimulation. Neurobiol. Dis. 2012, 46:314-324.
92. Leon S., Yin Y., Nguyen J., Irwin N., Benowitz L.I. Lens injury stimulates axon regeneration in the mature rat optic nerve. J. Neurosci. 2000, 20:4615-4626.
93. Li Y., Schlamp C.L., Poulsen K.P., Nickells R.W. Bax-dependent and independent pathways of retinal ganglion cell death induced by different damaging stimuli. Exp. Eye Res. 2000, 71:209-213.
94. Liedtke T., Schwamborn J.C., Schroer U., Thanos S. Elongation of axons during regeneration involves retinal crystallin {beta} b2 (crybb2). Mol. Cell Proteomics 2007, 6:895-907.
95. Lingor P., Koeberle P., Kugler S., Bahr M. Down-regulation of apoptosis mediators by RNAi inhibits axotomy-induced retinal ganglion cell death in vivo. Brain 2005, 128:550-558.
96. Lingor P., Teusch N., Schwarz K., Mueller R., Mack H., Bahr M., Mueller B.K. Inhibition of Rho kinase (ROCK) increases neurite outgrowth on chondroitin sulphate proteoglycan in vitro and axonal regeneration in the adult optic nerve in vivo. J. Neurochem. 2007, 103:181-189.
97. Lingor P., Tonges L., Pieper N., Bermel C., Barski E., Planchamp V., Bahr M. ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain 2008, 131:250-263.
98. Liu B.P., Fournier A., GrandPre T., Strittmatter S.M. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002, 297:1190-1193.
99. Logan A., Berry M. Cellular and molecular determinants of glial scar formation. Adv. Exp. Med. Biol. 2002, 513:115-158.
100. Logan A., Berry M., Gonzalez A.M., Frautschy S.A., Sporn M.B., Baird A. Effects of transforming growth factor beta 1 on scar production in the injured central nervous system of the rat. Eur. J. Neurosci. 1994, 6:355-363.
101. Logan A., Green J., Hunter A., Jackson R., Berry M. Inhibition of glial scarring in the injured rat brain by a recombinant human monoclonal antibody to transforming growth factor-beta2. Eur. J. Neurosci. 1999, 11:2367-2374.
102. Lorber B., Berry M., Logan A. Different factors promote axonal regeneration of adult rat retinal ganglion cells after lens injury and intravitreal peripheral nerve grafting. J. Neurosci. Res. 2008, 86:894-903.
103. Lorber B., Berry M., Douglas M.R., Nakazawa T., Logan A. Activated retinal glia promote neurite outgrowth of retinal ganglion cells via apolipoprotein E. J. Neurosci. Res. 2009.
104. Malik J.M., Shevtsova Z., Bahr M., Kugler S. Long-term in vivo inhibition of CNS neurodegeneration by Bcl-XL gene transfer. Mol. Ther. 2005, 11:373-381.
105. Manitt C., Colicos M.A., Thompson K.M., Rousselle E., Peterson A.C., Kennedy T.E. Widespread expression of netrin-1 by neurons and oligodendrocytes in the adult mammalian spinal cord. J. Neurosci. 2001, 21:3911-3922.
106. 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. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:1632-1636.
107. McKeon R.J., Schreiber R.C., Rudge J.S., Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J. Neurosci. 1991, 11:3398-3411.
108. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 1994, 13:805-811.
109. Mey J., Thanos S. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res. 1993, 602:304-317.
110. Mi S., Lee X., Shao Z., Thill G., Ji B., Relton J., Levesque M., Allaire N., Perrin S., Sands B., Crowell T., Cate R.L., McCoy J.M., Pepinsky R.B. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 2004, 7:221-228.
111. Mimura F., Yamagishi S., Arimura N., Fujitani M., Kubo T., Kaibuchi K., Yamashita T. Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. J. Biol. Chem. 2006, 281:15970-15979.
112. Monnier P.P., D'Onofrio P.M., Magharious M., Hollander A.C., Tassew N., Szydlowska K., Tymianski M., Koeberle P.D. Involvement of caspase-6 and caspase-8 in neuronal apoptosis and the regenerative failure of injured retinal ganglion cells. J. Neurosci. 2011, 31:10494-10505.
113. Moore D.L., Blackmore M.G., Hu Y., Kaestner K.H., Bixby J.L., Lemmon V.P., Goldberg J.L. KLF family members regulate intrinsic axon regeneration ability. Science 2009, 326:298-301.
114. Moreau-Fauvarque C., Kumanogoh A., Camand E., Jaillard C., Barbin G., Boquet I., Love C., Jones E.Y., Kikutani H., Lubetzki C., Dusart I., Chedotal A. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J. Neurosci. 2003, 23:9229-9239.
115. Mueller B.K. Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 1999, 22:351-388.
116. Mukhopadhyay G., Doherty P., Walsh F.S., Crocker P.R., Filbin M.T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 1994, 13:757-767.
117. Müller A., Hauk T.G., Fischer D. Astrocyte-derived CNTF switches mature RGCs to a regenerative state following inflammatory stimulation. Brain 2007, 130:3308-3320.
118. Müller A., Hauk T.G., Leibinger M., Marienfeld R., Fischer D. Exogenous CNTF stimulates axon regeneration of retinal ganglion cells partially via endogenous CNTF. Mol. Cell. Neurosci. 2009, 41:233-246.
119. Muzio M., Stockwell B.R., Stennicke H.R., Salvesen G.S., Dixit V.M. An induced proximity model for caspase-8 activation. J. Biol. Chem. 1998, 273:2926-2930.
120. Nicholson S.E., De Souza D., Fabri L.J., Corbin J., Willson T.A., Zhang J.G., Silva A., Asimakis M., Farley A., Nash A.D., Metcalf D., Hilton D.J., Nicola N.A., Baca M. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6493-6498.
121. Niederost B.P., Zimmermann D.R., Schwab M.E., Bandtlow C.E. Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J. Neurosci. 1999, 19:8979-8989.
122. Nishida K., Yoshida Y., Itoh M., Fukada T., Ohtani T., Shirogane T., Atsumi T., Takahashi-Tezuka M., Ishihara K., Hibi M., Hirano T. Gab-family adapter proteins act downstream of cytokine and growth factor receptors and T- and B-cell antigen receptors. Blood 1999, 93:1809-1816.
123. Oertle T., van der Haar M.E., Bandtlow C.E., Robeva A., Burfeind P., Buss A., Huber A.B., Simonen M., Schnell L., Brosamle C., Kaupmann K., Vallon R., Schwab M.E. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J. Neurosci. 2003, 23:5393-5406.
124. 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. J. Neurosci. 2004, 24:10806-10815.
125. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
126. Park K.K., Hu Y., Muhling J., Pollett M.A., Dallimore E.J., Turnley A.M., Cui Q., Harvey A.R. Cytokine-induced SOCS expression is inhibited by cAMP analogue: impact on regeneration in injured retina. Mol. Cell. Neurosci. 2009.
127. Perdigoto A.L., Chaudhry N., Barnes G.N., Filbin M.T., Carter B.D. A novel role for PTEN in the inhibition of neurite outgrowth by myelin-associated glycoprotein in cortical neurons. Mol. Cell. Neurosci. 2011, 46:235-244.
128. 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.
129. Pernet V., Joly S., Dalkara D., Schwarz O., Christ F., Schaffer D., Flannery J.G., Schwab M.E. Neuronal Nogo-A upregulation does not contribute to ER stress-associated apoptosis but participates in the regenerative response in the axotomized adult retina. Cell Death Differ. 2011.
130. Peterson W.M., Wang Q., Tzekova R., Wiegand S.J. Ciliary neurotrophic factor and stress stimuli activate the Jak-STAT pathway in retinal neurons and glia. J. Neurosci. 2000, 20:4081-4090.
131. Pettmann B., Henderson C.E. Neuronal cell death. Neuron 1998, 20:633-647.
132. Pignot V., Hein A.E., Barske C., Wiessner C., Walmsley A.R., Kaupmann K., Mayeur H., Sommer B., Mir A.K., Frentzel S. Characterization of two novel proteins, NgRH1 and NgRH2, structurally and biochemically homologous to the Nogo-66 receptor. J. Neurochem. 2003, 85:717-728.
133. Plant G.T. Optic neuritis and multiple sclerosis. Curr. Opin. Neurol. 2008, 21:16-21.
134. Prinjha R., Moore S.E., Vinson M., Blake S., Morrow R., Christie G., Michalovich D., Simmons D.L., Walsh F.S. Inhibitor of neurite outgrowth in humans. Nature 2000, 403:383-384.
135. Rabacchi S.A., Ensini M., Bonfanti L., Gravina A., Maffei L. Nerve growth factor reduces apoptosis of axotomized retinal ganglion cells in the neonatal rat. Neuroscience 1994, 63:969-973.
136. Rane S.G., Reddy E.P. Janus kinases: components of multiple signaling pathways. Oncogene 2000, 19:5662-5679.
137. Rao N.A., Kimoto T., Zamir E., Giri R., Wang R., Ito S., Pararajasegaram G., Read R.W., Wu G.S. Pathogenic role of retinal microglia in experimental uveoretinitis. Invest. Ophthalmol. Vis. Sci. 2003, 44:22-31.
138. Rimaniol A.C., Lekieffre D., Serrano A., Masson A., Benavides J., Zavala F. Biphasic transforming growth factor-beta production flanking the pro-inflammatory cytokine response in cerebral trauma. Neuroreport 1995, 7:133-136.
139. Sapieha P.S., Duplan L., Uetani N., Joly S., Tremblay M.L., Kennedy T.E., Di Polo A. Receptor protein tyrosine phosphatase sigma inhibits axon regrowth in the adult injured CNS. Mol. Cell. Neurosci. 2005, 28:625-635.
140. 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 Res. 2004, 1013:152-158.
141. Schallenberg M., Charalambous P., Thanos S. GM-CSF regulates the ERK1/2 pathways and protects injured retinal ganglion cells from induced death. Exp. Eye Res. 2009, 89:665-677.
142. Schmeer C., Straten G., Kugler S., Gravel C., Bahr 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. Eur. J. Neurosci. 2002, 15:637-643.
143. Sengottuvel V., Fischer D. Facilitating axon regeneration in the injured CNS by microtubules stabilization. Commun. Integr. Biol. 2011, 4:391-393.
144. Sengottuvel V., Leibinger M., Pfreimer M., Andreadaki A., Fischer D. Taxol facilitates axon regeneration in the mature CNS. J. Neurosci. 2011, 31:2688-2699.
145. Shen Y., Tenney A.P., Busch S.A., Horn K.P., Cuascut F.X., Liu K., He Z., Silver J., Flanagan J.G. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326:592-596.
146. Shouda T., Yoshida T., Hanada T., Wakioka T., Oishi M., Miyoshi K., Komiya S., Kosai K., Hanakawa Y., Hashimoto K., Nagata K., Yoshimura A. Induction of the cytokine signal regulator SOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J. Clin. Invest. 2001, 108:1781-1788.
147. Sievers J., Hausmann B., Unsicker K., Berry M. Fibroblast growth factors promote the survival of adult rat retinal ganglion cells after transection of the optic nerve. Neurosci. Lett. 1987, 76:157-162.
148. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
149. Sivakumar V., Foulds W.S., Luu C.D., Ling E.A., Kaur C. Retinal ganglion cell death is induced by microglia derived pro-inflammatory cytokines in the hypoxic neonatal retina. J. Pathol. 2011, 224:245-260.
150. Smith P.D., Sun F., Park K.K., Cai B., Wang C., Kuwako K., Martinez-Carrasco I., Connolly L., He Z. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 2009, 64:617-623.
151. So K.F., Aguayo A.J. Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats. Brain Res. 1985, 328:349-354.
152. Soto I., Pease M.E., Son J.L., Shi X., Quigley H.A., Marsh-Armstrong N. Retinal ganglion cell loss in a rat ocular hypertension model is sectorial and involves early optic nerve axon loss. Invest. Ophthalmol. Vis. Sci. 2011, 52:434-441.
153. Stahl N., Boulton T.G., Farruggella T., Ip N.Y., Davis S., Witthuhn B.A., Quelle F.W., Silvennoinen O., Barbieri G., Pellegrini S., et al. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 beta receptor components. Science 1994, 263:92-95.
154. Su Y., Wang F., Teng Y., Zhao S.G., Cui H., Pan S.H. Axonal regeneration of optic nerve after crush in Nogo66 receptor knockout mice. Neurosci. Lett. 2009, 460:223-226.
155. Sun F., Park K.K., Belin S., Wang D., Lu T., Chen G., Zhang K., Yeung C., Feng G., Yankner B.A., He Z. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011, 480:372-375.
156. Tang B.L. Inhibitors of neuronal regeneration: mediators and signaling mechanisms. Neurochem. Int. 2003, 42:189-203.
157. Thanos S., Mey J., Wild M. Treatment of the adult retina with microglia-suppressing factors retards axotomy-induced neuronal degradation and enhances axonal regeneration in vivo and in vitro. J. Neurosci. 1993, 13:455-466.
158. Tonges L., Ostendorf T., Lamballe F., Genestine M., Dono R., Koch J.C., Bahr M., Maina F., Lingor P. Hepatocyte growth factor protects retinal ganglion cells by increasing neuronal survival and axonal regeneration in vitro and in vivo. J. Neurochem. 2011, 117:892-903.
159. Vidal-Sanz M., Bray G.M., Villegas-Perez M.P., Thanos S., Aguayo A.J. Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J. Neurosci. 1987, 7:2894-2909.
160. Vidal-Sanz M., Villegas-Perez M.P., Bray G.M., Aguayo A.J. Persistent retrograde labeling of adult rat retinal ganglion cells with the carbocyanine dye diI. Exp. Neurol. 1988, 102:92-101.
161. Vidal-Sanz M., Salinas-Navarro M., Nadal-Nicolas F.M., Alarcon-Martinez L., Valiente-Soriano F.J., Miralles de Imperial J., Aviles-Trigueros M., Agudo-Barriuso M., Villegas-Perez M.P. Understanding glaucomatous damage: anatomical and functional data from ocular hypertensive rodent retinas. Prog. Retin. Eye Res. 2011.
162. Wang K.C., Kim J.A., Sivasankaran R., Segal R., He Z. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002, 420:74-78.
163. Wang K.C., Koprivica V., Kim J.A., Sivasankaran R., Guo Y., Neve R.L., He Z. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002, 417:941-944.
164. Weishaupt J.H., Diem R., Kermer P., Krajewski S., Reed J.C., Bahr M. Contribution of caspase-8 to apoptosis of axotomized rat retinal ganglion cells in vivo. Neurobiol. Dis. 2003, 13:124-135.
165. Winzeler A.M., Mandemakers W.J., Sun M.Z., Stafford M., Phillips C.T., Barres B.A. The lipid sulfatide is a novel myelin-associated inhibitor of CNS axon outgrowth. J. Neurosci. 2011, 31:6481-6492.
166. Wistow G. Identification of lens crystallins: a model system for gene recruitment. Methods Enzymol. 1993, 224:563-575.
167. Witte H., Neukirchen D., Bradke F. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 2008, 180:619-632.
168. Wohl S.G., Schmeer C.W., Witte O.W., Isenmann S. Proliferative response of microglia and macrophages in the adult mouse eye after optic nerve lesion. Invest. Ophthalmol. Vis. Sci. 2010, 51:2686-2696.
169. Wong S.T., Henley J.R., Kanning K.C., Huang K.H., Bothwell M., Poo M.M. A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 2002, 5:1302-1308.
170. Yamashita T., Higuchi H., Tohyama M. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 2002, 157:565-570.
171. Yin Y., Cui Q., Li Y., Irwin N., Fischer D., Harvey A.R., Benowitz L.I. Macrophage-derived factors stimulate optic nerve regeneration. J. Neurosci. 2003, 23:2284-2293.
172. Yiu G., He Z. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 2006, 7:617-627.
173. Zhang C.W., Lu Q., You S.W., Zhi Y., Yip H.K., Wu W., So K.F., Cui Q. CNTF and BDNF have similar effects on retinal ganglion cell survival but differential effects on nitric oxide synthase expression soon after optic nerve injury. Invest. Ophthalmol. Vis. Sci. 2005, 46:1497-1503.