Combined application of BDNF to the eye and brain enhances ganglion cell survival and function in the cat after optic nerve injury

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 1, 2010, Pages 327-334

  Weber, Arthur J ^a   Viswanáthan, Suresh ^b   Ramanathan, Chidambaram ^a   Harman, Christine D ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROPROTECTIVE AGENT; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAT; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; ELECTRORETINOGRAPHY; FEMALE; MALE; NERVE CRUSH; NEUROPROTECTION; NONHUMAN; OPTIC NERVE INJURY; PRIORITY JOURNAL; RETINA GANGLION CELL; ANIMAL; CELL COUNT; DISEASE MODEL; INJECTION; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA DEGENERATION; VISUAL CORTEX; VITREOUS BODY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CATS; CELL COUNT; CELL SURVIVAL; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; FEMALE; INJECTIONS; MALE; NERVE CRUSH; NEUROPROTECTIVE AGENTS; OPTIC NERVE INJURIES; RECOMBINANT PROTEINS; RETINAL DEGENERATION; RETINAL GANGLION CELLS; VISUAL CORTEX; VITREOUS BODY;

EID: 75749108972     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-3740     Document Type: Article

References (58)

1. Kalil RE. Removal of visual cortex in the cat: effects on the morphological development of the retino-geniculo-cortical pathway. In: Stone J, Dreher B, Rapaport D, eds. Development of Visual Pathways in Mammals: Proceedings of a satellite symposium of the XXIX International Congress of the Union of Physiological Sciences, Sydney, Australia, August 24-27, 1983. New York: Alan R. Liss; 1984:257-274.
2. Pearson HE, Labar DR, Payne BR, Cornwell P, Aggarwal N. Transneuronal retrograde degeneration in the cat retina following neonatal ablation of visual cortex. Brain Res. 1981;212:470-475.
3. Weber AJ, Kalil RE, Stanford LR. Morphology of single, physiologically identified Y retinogeniculate axons in the cat following damage to visual cortex at birth. J Comp Neurol. 1989;289:446-455.
4. Pearson HE, Sonstein WJ, Stoffler DJ. Selectivity of kainic acid as a neurotoxin within the dorsal lateral geniculate nucleus of the cat: a model for transneuronal retrograde degeneration. J Neurocytol. 1991;20:376-386.
5. Pearson HE, Stoffler DJ. Retinal ganglion cell degeneration following loss of postsynaptic target neurons in the dorsal lateral geniculate nucleus of the adult cat. Exp Neurol. 1992;116:163-171.
6. Chaum E. Retinal neuroprotection by growth factors: a mechanistic perspective. J Cell Biochem. 2003;88:57-75.
7. Lebrun-Julien F, DiPolo A. Molecular and cell-based approaches for neuroprotection in glaucoma. Optometry Vis Sci. 2008;85:E417-E424.
8. Harvey AR, Hu Y, Leaver SG, et al. Gene therapy and transplantation in CNS repair: the visual system. Prog Retin Eye Res. 2006;25:449-489.
9. Chen H, Weber AJ. BDNF enhances retinal ganglion cell survival in cats with optic nerve damage. Invest Ophthalmol Vis Sci. 2001;42:966-974.
10. Cheng L, Sapieha P, Kittlerova P, Hauswirth WW, Di Polo A. TrkB gene transfer protects retinal ganglion cells from axotomy-induced death in vivo. J Neurosci. 2002;22:3977-3986.
11. 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;95:3978-3983.
12. Klöcker N, Kermer P, Weishaupt JH, Labes M, Ankerhold R, Bahr M. Brain-derived neurotrophic factor-mediated neuroprotection of adult rat retinal ganglion cells in vivo does not exclusively depend on phosphatidyl-inositol-3'-kinase/protein kinase B signaling. J Neurosci. 2000;20:6962-6967.
13. Mansour-Robaey S, Clarke DB, Wang YC, 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;91:1632-1636.
14. 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.
15. Nakazawa T, Tamai M, Mori N. Brain-derived neurotrophic factor prevents axotomized retinal ganglion cell death through MAPK and PI3K signaling pathways. Invest Ophthalmol Vis Sci. 2002;43:3319-3326.
16. Peinado-Ramon P, Salvador M, Villegas-Perez 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;37:489-500.
17. Weber AJ, Harman CD. BDNF Preserves the dendritic morphology of α and β ganglion cells in the cat retina after optic nerve injury. Invest Ophthalmol Vis Sci. 2008;49:2456-2463.
18. Weber AJ, Harman CD, Viswanathan S. Effects of optic nerve injury, glaucoma, and neuroprotection on the survival, structure, and function of ganglion cells in the mammalian retina. J Physiol. 2008;586:4393-4400.
19. Chen H, Weber AJ. 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.
20. Frank L, Ventimiglia R, Anderson K, Lindsay R, Rudge J. BDN F down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. Eur J Neurosc. 1996;8:1220-1230.
21. Frank L, Wiegand SJ, Siuciak JA, Lindsay RM, Rudge JS. Effects of BDNF infusion on the regulation of TrkB protein and message in adult rat brain. Exp Neurol. 1997;145:62-70.
22. Knusel B, Gao H, Okazaki T, et al. Ligand-induced down-regulation of trk messenger RNA, protein and tyrosine phosphorylation in rat cortical neurons. Neuroscience. 1997;78:851-862.
23. Sommerfeld MT, Schweigreiter R, Barde YA, Hoppe E. Downregulation of the neurotrophin receptor TrkB following ligand binding: evidence for an involvement of the proteasome and differential regulation of TrkA and TrkB. J Biol Chem. 2000;275:8982-8990.
24. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci. 2000;20:4615-4626.
25. Tusa RJ, Palmer LA, Rosenquist AC. The retinotopic organization of area 17 (striate cortex) in the cat. J Comp Neurol. 1978;177:213-236.
26. Fernald R, Chase R. An improved method for plotting retinal landmarks and focusing the eyes. Vision Res. 1971;11:95-96.
27. Hess RF, Baker CL, Zrenner E, Schwarzer J. Differences between electroretinograms of cat and primate. Neurophysiology. 1986;56:747-768.
28. Boycott BB, Wässle H. The morphological types of ganglion cells of the domestic cat's retina. J Physiol. 1974;240:397-419.
29. Stone J. The number and distribution of ganglion cells in the cat's retina. J Comp Neurol. 1978;180:753-771.
30. Vakkur GJ, Bishop PO, Kozak W. Visual optics in the cat, including posterior nodal distance and retinal landmarks. Vision Res. 1963;61:289-314.
31. Stone J. A quantitative analysis of the distribution of ganglion cells in the cat's retina. J Comp Neurol. 1965;124:337-352.
32. Berson DM, Isayama T, Pu M. The eta ganglion cell type of cat retina. J Comp Neurol. 1999;408:204-219.
33. Berson DM, Pu M, Famiglietti EV. The zeta cell: a new ganglion cell type in cat retina. J Comp Neurol. 1998;399:269-288.
34. Isayama T, Berson DM, Pu M. Theta ganglion cell type of cat retina. J Comp Neurol. 2000;417:32-48.
35. Hughes A. Population magnitudes and distribution of the major modal classes of cat retinal ganglion cell as estimated from HRP filling and a systematic survey of the soma diameter spectra for classical neurones. J Comp Neurol. 1981;197:303-339.
36. Wong RO, Hughes A. The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina. J Comp Neurol. 1987;255:159-177.
37. Naito J. Course of retinogeniculate projection fibers in the cat optic nerve. J Comp Neurol. 1986;251:376-387.
38. Stein JJ, Johnson SA, Berson DA. Distribution and coverage of beta cells in the cat retina. J Comp Neurol. 1996;372:597-617.
39. Viswanathan S, Frishman LJ, Robson JG. The uniform field and pattern ERG in macaques with experimental glaucoma: removal of spiking activity. Invest Ophthalmol Vis Sci. 2000;41:2797-2810.
40. Yoles E, Schwartz M. Elevation of intraocular glutamate levels in rats with partial lesion of the optic nerve. Arch Ophthalmol. 1998;116:906-910.
41. Kafitz KW, Rose CR, Thoenen H, Konnerth A. Neurotrophinevoked rapid excitation through TrkB receptors. Nature. 1999;401:918-921.
42. 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;21:681-693.
43. Altar C, Cai N, Bliven T, et al. Anterograde transport of brainderived neurotrophic factor and its role in the brain. Nature. 1997;389:856-860.
44. Caleo M, Medini P, von Bartheld C, Maffei L. Provision of brainderived neurotrophic factor via anterograde transport from the eye preserves the physiological responses of axotomized geniculate neurons. J Neurosci. 2003;23:287-296.
45. Caleo M, Menna E, Chierzi S, Cenni M, Maffei L. Brain-derived neurotrophic factor is an anterograde survival factor in the rat visual system. Curr Biol. 2000;10:1155-1161.
46. Fawcett JP, Bamji SX, Causing CG, et al. Functional evidence that BDNF is an anterograde neuronal trophic factor in the CNS. J Neurosci. 1998;18:2808-2821.
47. Nagappan G, Lu B. Activity-dependent modulation of the BDNF receptor TrkB: mechanisms and implications. Trends Neurosci. 2005;28:464-471.
48. Cui Q, Tang LS, Hu B, So KF, Yip HK. Expression of trkA, trkB, and trkC in injured and regenerating retinal ganglion cells of adult rats. Invest Ophthalmol Vis Sci. 2002;43:1954-1964.
49. Weber AJ, Harman CD. Structure-function relations of parasol cells in the normal and glaucomatous primate retina. Invest Ophthalmol Vis Sci. 2005;46:3197-3207.
50. Eide FF, Vining ER, Eide BL, Zang K, Wang XY, Reichardt LF. Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci. 1996;16:3123-3129.
51. Gilbert CD, Kelly JP. The projection of cells in different layers of the cat's visual cortex. J Comp Neurol. 1975;163:81-106.
52. Kawamura S, Sprague JM, Niimi K. Corticofugal projections from the visual cortices to the thalamus, pretectum, and superior colliculus in the cat. J Comp Neurol. 1974;158:339-362.
53. Updyke BV. Topographic organization of the projection from cortical area 17, 18, and 19 onto the thalamus, pretectum and superior colliculus in the cat. J Comp Neurol. 1977;173:81-122.
54. Weber AJ, Kalil RE. Development of corticogeniculate synapses in the cat. J Comp Neurol. 1987;264.
55. Watanabe M, Inukai N, Fukuda Y. Survival of retinal ganglion cells after transection of the optic nerve in adult cats: a quantitative study within two weeks. Vis Neurosci. 2001;18:137-145.
56. Watanabe M, Tokita Y, Kato M, Fukuda Y. Intravitreal injections of neurotrophic factors and forskolin enhance survival and axonal regeneration of axotomized beta ganglion cells in cat retina. Neuroscience. 2003;116:733-742.
57. Donovan A. The nerve fiber composition of the cat optic nerve. J Anat. 1967;101:1-11.
58. Hughes A, Wässle H. The cat optic nerve: fibre total count and diameter spectrum. J Comp Neurol. 1976;169:171-184.