Optic nerve regeneration

Archives of Ophthalmology

Volumn 128, Issue 8, 2010, Pages 1059-1064

  Benowitz, Larry I ^a   Yin, Yuqin ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; MANNOSE; ONCOMODULIN;

CELL STIMULATION; HUMAN; NERVE FIBER REGENERATION; NONHUMAN; OPTIC NERVE; OPTIC NERVE DISEASE; OPTIC NERVE FIBER; PRIORITY JOURNAL; RETINA GANGLION CELL; REVIEW; VISUAL IMPAIRMENT;

ANIMALS; AXONS; CALCIUM-BINDING PROTEINS; CYCLIC AMP; HUMANS; MANNOSE; NERVE REGENERATION; OPTIC NERVE; OPTIC NERVE INJURIES; RETINAL GANGLION CELLS;

EID: 77955450730     PISSN: 00039950     EISSN: 15383601     Source Type: Journal    
DOI: 10.1001/archophthalmol.2010.152     Document Type: Review

References (91)

1. Ramon y Cajal S. Degeneration and Regeneration of the Nervous System. Vol 5. New York, NY: Oxford University Press; 1991.
2. Aguayo AJ, Rasminsky M, Bray GM, et al. Degenerative and regenerative responses of injured neurons in the central nervous system of adult mammals. Philos Trans R Soc Lond B Biol Sci. 1991;331(1261):337-343.
3. Carbonetto S, Evans D, Cochard P. Nerve fiber growth in culture on tissue substrata from central and peripheral nervous systems. J Neurosci. 1987;7(2): 610-620. (Pubitemid 17017488)
4. Savio T, Schwab ME. Rat CNS white matter, but not gray matter, is nonpermissive for neuronal cell adhesion and fiber outgrowth. J Neurosci. 1989;9(4): 1126-1133.
5. Schwab ME, Thoenen H. Dissociated neurons regenerate into sciatic but not optic nerve explants in culture irrespective of neurotrophic factors. J Neurosci. 1985; 5(9):2415-2423. (Pubitemid 15226933)
6. 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(2):147-170.
7. Lazarov-Spiegler O, Solomon AS, Zeev-Brann AB, Hirschberg DL, Lavie V, Schwartz M. Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J. 1996;10(11):1296-1302.
8. Lazarov-Spiegler O, Solomon AS, Schwartz M. Peripheral nerve-stimulated macrophages simulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia. 1998;24(3):329-337. (Pubitemid 28465980)
9. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci. 2000;20(12):4615-4626.
10. Yin Y, Cui Q, Li Y, et al. Macrophage-derived factors stimulate optic nerve regeneration. J Neurosci. 2003;23(6):2284-2293.
11. Yin Y, Henzl MT, Lorber B, et al. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci. 2006;9(6):843-852.
12. Yin Y, Cui Q, Gilbert H, et al. Oncomodulin links inflammation to optic nerve regeneration. Proc Natl Acad Sci U S A. 2009;106(46):19587-19592.
13. Fischer D, Petkova V, Thanos S, Benowitz LI. Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J Neurosci. 2004;24(40):8726-8740.
14. Fischer D, Heiduschka P, Thanos S. Lens-injury-stimulated axonal regeneration throughout the optic pathway of adult rats. Exp Neurol. 2001;172(2):257-272. (Pubitemid 34075076)
15. Jo S, Wang E, Benowitz LI. Ciliary neurotrophic factor is an axogenesis factor for retinal ganglion cells. Neuroscience. 1999;89(2):579-591. (Pubitemid 29044338)
16. 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(4):894-903.
17. Li Y, Irwin N, Yin Y, Lanser M, Benowitz LI. Axon regeneration in goldfish and rat retinal ganglion cells: differential responsiveness to carbohydrates and cAMP. J Neurosci. 2003;23(21):7830-7838.
18. Hauk TG, 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(2):469-482.
19. Müller A, Hauk TG, Fischer D. Astrocyte-derived CNTF switches mature RGCs to a regenerative state following inflammatory stimulation. Brain. 2007;130(pt 12): 3308-3320. (Pubitemid 350209074)
20. Cui Q, Benowitz L, Yin Y. Does CNTF mediate the effect of intraocular inflammation on optic nerve regeneration? Brain. 2008;131(pt 6):e96-e97. doi:10.1093/brain/awn027.
21. 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(12):3943-3954.
22. Irwin N, Li Y-M, O'Toole JE, Benowitz LI. Mst3b, a purine-sensitive Ste20-like protein kinase, regulates axon outgrowth. Proc Natl Acad Sci U S A. 2006; 103(48):18320-18325.
23. Lorber B, Howe ML, Benowitz LI, Irwin N. Mst3b, an Ste20-like kinase, regulates axon regeneration in the mature CNS and PNS. Nat Neurosci. 2009;12 (11):1407-1414.
24. Park KK, Liu K, Hu Y, et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science. 2008;322(5903):963-966.
25. Smith PD, Sun F, Park KK, et al. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron. 2009;64(5):617-623.
26. Goldberg JL, Klassen MP, Hua Y, Barres BA. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science. 2002;296(5574):1860-1864.
27. Moore DL, Blackmore MG, Hu Y, et al. KLF family members regulate intrinsic axon regeneration ability. Science. 2009;326(5950):298-301.
28. Ming G-L, Song H-J, Berninger B, Holt CE, Tessier-Lavigne M, Poo M-M. cAMP-dependent growth cone guidance by netrin-1. Neuron. 1997;19(6):1225-1235. (Pubitemid 28030542)
29. Song H, Ming G, He Z, et al. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science. 1998;281(5382):1515-1518.
30. Meyer-Franke A, Wilkinson GA, Kruttgen A, et al. Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron. 1998;21(4):681-693.
31. Cai D, Deng K, Mellado W, Lee J, Ratan R, Filbin M. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron. 2002;35(4):711-719. (Pubitemid 35223030)
32. Park KK, Hu Y, Muhling J, et al. Cytokine-induced SOCS expression is inhibited by cAMP analogue: impact on regeneration in injured retina. Mol Cell Neurosci. 2009;41(3):313-324.
33. Deng K, He H, Qiu J, Lorber B, Bryson JB, Filbin MT. Increased synthesis of spermidine as a result of upregulation of arginase I promotes axonal regeneration in culture and in vivo. J Neurosci. 2009;29(30):9545-9552.
34. Monsul NT, Geisendorfer AR, Han PJ, et al. Intraocular injection of dibutyryl cyclic AMP promotes axon regeneration in rat optic nerve. Exp Neurol. 2004; 186(2):124-133.
35. Cui Q, Yip HK, Zhao RCH, So K-F, Harvey AR. Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol Cell Neurosci. 2003;22(1):49-61.
36. Müller A, Hauk TG, Leibinger M, Marienfeld R, Fischer D. Exogenous CNTF stimulates axon regeneration of retinal ganglion cells partially via endogenous CNTF. Mol Cell Neurosci. 2009;41(2):233-246.
37. Yin Y, Kurimoto T, Cen L, Gilbert H, Yang Y, Benowitz LI. Oncomodulin and cAMP interact in multiple ways to promote optic nerve regeneration. In: Program and abstracts of the Society for Neuroscience Annual Meeting; October 17-21, 2009; Chicago, Illinois. Program 32.11.
38. Villegas-Pérez MP, Vidal-Sanz M, Bray GM, Aguayo AJ. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci. 1988;8(1):265-280.
39. Chierzi S, Cenni MC, Maffei L, et al. Protection of retinal ganglion cells and preservation of function after optic nerve lesion in bcl-2 transgenic mice. Vision Res. 1998;38(10):1537-1543.
40. Malik JMI, Shevtsova Z, Bähr M, Kügler S. Long-term in vivo inhibition of CNS neurodegeneration by Bcl-XL gene transfer. Mol Ther. 2005;11(3):373-381. (Pubitemid 40277313)
41. Goldberg JL, Espinosa JS, Xu Y, Davidson N, Kovacs GTA, Barres BA. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron. 2002;33(5):689-702.
42. 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(2):304-317. (Pubitemid 23053202)
43. Weise J, Isenmann S, Klöcker N, et al. Adenovirus-mediated expression of ciliary neurotrophic factor (CNTF) rescues axotomized rat retinal ganglion cells but does not support axonal regeneration in vivo. Neurobiol Dis. 2000;7(3):212-223.
44. Mansour-Robaey S, Clarke DB, Wang Y-C, Bray GM, Aguayo AJ. 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(5):1632-1636.
45. Di Polo A, Aigner LJ, Dunn RJ, Bray GM, Aguayo AJ. Prolonged delivery of brain-derived neurotrophic factor by adenovirus-infected Müller cells temporarily rescues injured retinal ganglion cells. Proc Natl Acad Sci U S A. 1998;95(7):3978-3983. (Pubitemid 28173239)
46. Cohen A, Bray GM, Aguayo AJ. Neurotrophin-4/5 (NT-4/5) increases adult rat retinal ganglion cell survival and neurite outgrowth in vitro. J Neurobiol. 1994; 25(8):953-959.
47. Peinado-Ramón P, Salvador M, Villegas-Peréz MP, 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. Invest Ophthalmol Vis Sci. 1996;37(4):489-500.
48. Carmignoto G, Maffei L, Candeo P, Canella R, Comelli C. Effect of NGF on the survival of rat retinal ganglion cells following optic nerve section. J Neurosci. 1989;9(4):1263-1272. (Pubitemid 19116746)
49. Kermer P, Klöcker N, Labes M, Bähr 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. J Neurosci. 2000;20(2):2-8.
50. Frank T, Schlachetzki JCM, Göricke B, et al. Both systemic and local application of granulocyte-colony stimulating factor (G-CSF) is neuroprotective after retinal ganglion cell axotomy. BMC Neurosci. 2009;10:49-58.
51. Koeberle PD, Ball AK. Effects of GDNF on retinal ganglion cell survival following axotomy. Vision Res. 1998;38(10):1505-1515.
52. Yan Q, Wang J, Matheson CR, Urich JL. 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). J Neurobiol. 1999;38(3):382-390.
53. Koeberle PD, Ball AK. 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(3):555-567.
54. 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(pt 4):1014-1026.
55. Kermer P, Klöcker N, Labes M, Bähr M. Inhibition of CPP32-like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo. J Neurosci. 1998;18(12):4656-4662. (Pubitemid 28280174)
56. Kermer P, Klöcker N, Bähr M. Long-term effect of inhibition of ced 3-like caspases on the survival of axotomized retinal ganglion cells in vivo. Exp Neurol. 1999; 158(1):202-205.
57. Kermer P, Ankerhold R, Klöcker N, Krajewski S, Reed JC, Bähr M. Caspase-9: involvement in secondary death of axotomized rat retinal ganglion cells in vivo. Brain Res Mol Brain Res. 2000;85(1-2):144-150. (Pubitemid 32056245)
58. Weishaupt JH, Diem R, Kermer P, Krajewski S, Reed JC, Bähr M. Contribution of caspase-8 to apoptosis of axotomized rat retinal ganglion cells in vivo. Neurobiol Dis. 2003;13(2):124-135. (Pubitemid 36793977)
59. Weise J, Isenmann S, Bähr M. Increased expression and activation of poly(ADP-ribose) polymerase (PARP) contribute to retinal ganglion cell death following rat optic nerve transection. Cell Death Differ. 2001;8(8):801-807.
60. Koeberle PD, Ball AK. Nitric oxide synthase inhibition delays axonal degeneration and promotes the survival of axotomized retinal ganglion cells. Exp Neurol. 1999;158(2):366-381.
61. Swanson KI, Schlieve CR, Lieven CJ, Levin LA. Neuroprotective effect of sulfhydryl reduction in a rat optic nerve crush model. Invest Ophthalmol Vis Sci. 2005; 46(10):3737-3741.
62. Sanders EJ, Parker E, Harvey S. Retinal ganglion cell survival in development: mechanisms of retinal growth hormone action. Exp Eye Res. 2006;83(5):1205-1214. (Pubitemid 44397041)
63. Cheung ZH, Leung MCP, Yip HK, Wu W, Siu FKW, So K-F. A neuroprotective herbal mixture inhibits caspase-3-independent apoptosis in retinal ganglion cells. Cell Mol Neurobiol. 2008;28(1):137-155.
64. Fitzgerald M, Payne SC, Bartlett CA, Evill L, Harvey AR, Dunlop SA. Secondary retinal ganglion cell death and the neuroprotective effects of the calcium channel blocker lomerizine. Invest Ophthalmol Vis Sci. 2009;50(11):5456-5462.
65. Sapieha PS, Peltier M, Rendahl KG, Manning WC, Di Polo A. Fibroblast growth factor-2 gene delivery stimulates axon growth by adult retinal ganglion cells after acute optic nerve injury. Mol Cell Neurosci. 2003;24(3):656-672.
66. Cui Q, Lu Q, So KF, Yip HK. CNTF, not other trophic factors, promotes axonal regeneration of axotomized retinal ganglion cells in adult hamsters. Invest Ophthalmol Vis Sci. 1999;40(3):760-766. (Pubitemid 29109456)
67. Logan A, Ahmed Z, Baird A, Gonzalez AM, Berry M. Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain. 2006;129(pt 2):490-502.
68. Leibinger M, Müller A, Andreadaki A, Hauk TG, 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(45):14334-14341.
69. Lingor P, Tönges L, Pieper N, et al. ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain. 2008;131(pt 1):250-263.
70. Lorber B, Berry M, Logan A, Tonge D. Effect of lens lesion on neurite outgrowth of retinal ganglion cells in vitro. Mol Cell Neurosci. 2002;21(2):301-311.
71. Cui Q, Harvey AR. CNTF promotes the regrowth of retinal ganglion cell axons into murine peripheral nerve grafts. Neuroreport. 2000;11(18):3999-4002. (Pubitemid 32038792)
72. Cen L-P, Luo J-M, Zhang C-W, et al. Chemotactic effect of ciliary neurotrophic factor on macrophages in retinal ganglion cell survival and axonal regeneration. Invest Ophthalmol Vis Sci. 2007;48(9):4257-4266.
73. Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci. 2003;4(9):703-713. (Pubitemid 37280150)
74. Cafferty WBJ, McGee AW, Strittmatter SM. Axonal growth therapeutics: regeneration or sprouting or plasticity? Trends Neurosci. 2008;31(5):215-220.
75. Rossignol S, Schwab M, Schwartz M, Fehlings MG. Spinal cord injury: time to move? J Neurosci. 2007;27(44):11782-11792. (Pubitemid 350072087)
76. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci. 2004; 5(2):146-156.
77. Goldberg JL, Vargas ME, Wang JT, et al. An oligodendrocyte lineage-specific semaphorin, Sema5A, inhibits axon growth by retinal ganglion cells. J Neurosci. 2004; 24(21):4989-4999.
78. Chierzi S, Strettoi E, Cenni MC, Maffei L. Optic nerve crush: axonal responses in wild-type and bcl-2 transgenic mice. J Neurosci. 1999;19(19):8367-8376.
79. Fischer D, He Z, Benowitz LI. Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J Neurosci. 2004;24(7):1646-1651.
80. Lehmann M, Fournier A, Selles-Navarro I, et al. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J Neurosci. 1999;19(17):7537-7547.
81. Bertrand J, Winton MJ, Rodriguez-Hernandez N, Campenot RB, 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(5):1113-1121.
82. Battisti WP, Shinar Y, Schwartz M, Levitt P, Murray M. Temporal and spatial patterns of expression of laminin, chondroitin sulphate proteoglycan and HNK-1 immunoreactivity during regeneration in the goldfish optic nerve. J Neurocytol. 1992; 21(8):557-573.
83. Ahmed Z, Dent RG, Leadbeater WE, Smith C, Berry M, Logan A. Matrix metalloproteases: degradation of the inhibitory environment of the transected optic nerve and the scar by regenerating axons. Mol Cell Neurosci. 2005;28(1):64-78. (Pubitemid 39656012)
84. Haupt C, Huber AB. How axons see their way: axonal guidance in the visual system. Front Biosci. 2008;13:3136-3149.
85. Erskine L, Herrera E. The retinal ganglion cell axon's journey: insights into molecular mechanisms of axon guidance. Dev Biol. 2007;308(1):1-14.
86. McLaughlin T, O'Leary DD. Molecular gradients and development of retinotopic maps. Annu Rev Neurosci. 2005;28:327-355. (Pubitemid 41098909)
87. Wizenmann A, Thies E, Klostermann S, Bonhoeffer F, Bähr M. Appearance of targetspecific guidance information for regenerating axons after CNS lesions. Neuron. 1993;11(5):975-983.
88. Bähr M, Wizenmann A. Retinal ganglion cell axons recognize specific guidance cues present in the deafferented adult rat superior colliculus. J Neurosci. 1996; 16(16):5106-5116. (Pubitemid 26269670)
89. Wizenmann A, Bähr M. Growth preferences of adult rat retinal ganglion cell axons in retinotectal cocultures. J Neurobiol. 1998;35(4):379-387.
90. Keirstead SA, Rasminsky M, Fukuda Y, Carter DA, Aguayo AJ, Vidal-Sanz M. Electrophysiologic responses in hamster superior colliculus evoked by regenerating retinal axons. Science. 1989;246(4927):255-257. (Pubitemid 19264640)
91. Steward O, Zheng B, Tessier-Lavigne M. False resurrections: distinguishing regenerated from spared axons in the injured central nervous system. J Comp Neurol. 2003;459(1):1-8.