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 and Visual Science

Volumn 37, Issue 4, 1996, Pages 489-500

  Peinado Ramón, Paloma ^b   Salvador, Mercedes ^b   Villegas Pérez, María P ^b   Vidal Sanz, Manuel ^b  

^a UNIVERSITY OF MURCIA   (Spain)

^b NONE

Author keywords

adult rat retina; axotomy; neuronal degeneration; neurotrophins; retinal ganglion cells

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN 3; NEUROTROPHIN 4;

ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL;

ANIMALS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL COUNT; CELL DEATH; CELL SURVIVAL; DENERVATION; FEMALE; FLUORESCENT DYES; INJECTIONS; MICROSCOPY, FLUORESCENCE; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUROTROPHIN 3; OPTIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; STILBAMIDINES;

EID: 0029979673     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Villegas-Pérez MP, Vidal-Sanz M, Rasminsky M, Bray GM, Aguayo AJ. Rapid and protracted phases of retinal ganglion cells loss follow axotomy in the optic nerve of adult rats. J Neurobiol. 1993;24:23-36
2. 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;8:265-280.
3. Baird A, Normède P, Böhlen P. Immunoreactive fibroblast growth factor in cells of peritoneal exudate suggests its identity with macrophage-derived growth factor. Biochem Biophys Res Commun. 1985;126:358-364.
4. Manthorpe M, Skaper SD, Williams LR, Varon S. Purification of adult rat sciatic nerve ciliary neurono-trophic factor. Brain Res. 1986; 367:282-286.
5. Stöckli KA, Lottspeich F, Sendtner M, et al. Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature. 1989;342:920-923.
6. Heümann R, Lindholm D, Bandtlow C, et al. Differential regulation of nerve growth factor (NGF) and NGF-receptor mRNA in the rat sciatic nerve during development, degeneration and regeneration: Role played by macrophages. Proc Natl Acad Sci USA. 1987; 84:8735-8739.
7. Taniuchi M, Clark HB, Schweitzer JB, Johnson EM Jr. Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: Ultrastructural location, suppression by axonal contact, and binding properties. J Neurosa. 1988;8:664-681.
8. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H. Enhanced synthesis of brain-derived neurotrophicfactor in the lesioned peripheral nerve: Different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol. 1992; 119:45-54.
9. Funakoshi H, Frisèn J, Barbany G, et al. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol. 1993; 123:455-465.
10. Hallböök F, Ibañez CF, Persson H. Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron. 1991;6:845-858.
11. Berkemeier L, Windsow J, Raplan D, Nikolics K, Goeddel D, Rosenthal A. Neurotrophin-5: A novel neurotropic factor that activates trk and trkB. Neuron. 1991; 7:857-866.
12. Ip N, Ibánez C, Nye S, et al. Mammalian neurotrophin-4: Structure, distribution and receptor specificity. Proc Natl Acad Sci USA. 1992;89:3060-3064.
13. Hohn A, Leibrock J, Bailey K, Barde YA. Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature. 1990;344:339-341.
14. Ernfors P, Ibáñez CF, Ebendal T, et al. Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: Developmental and topographical expression in the brain. Proc Natl Acad Sci USA. 1990;87:5454-5458.
15. Maisonpierre PC, Belluscio L, Squinto S, et al. Neurotrophin-3: A neurotrophic factor related to NGF and BDNF. Science. 1990;247:1446-1451.
16. Barde YA., Edgar D, Thoenen H. Purification of a new neurotrophic factor from the mammalian brain. EMBO J. 1982;5:549-553.
17. Klein R, Naduri V, Jing SA, et al. The trkB tyrosine kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell. 1991;66:395-403.
18. Squinto SP, Suit TN, Aldrich TH, et al. TrkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell. 1991;65:885-893.
19. Klein R, Lamballe F, Bryant S, Barbacid M. The trkB tyrosine protein kinase is a receptor for neurotrophin-4. Neuron. 1992;8:947-956.
20. Ernfors P, Merlio JP, Persson H. Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur J Neurosci. 1992; 4:1140-1158.
21. Allendoerfer KL, Cabelli RJ, Escandón E, Kaplan DR, Nikolics K, Shatz CJ. Regulation of neurotrophin receptors during the maturation of the mammalian visual system. J Neurosci. 1994; 14:1795-1811.
22. Pérez M-TR, Caminos E. Expression of brain-derived neurotrophic factor and of its functional receptor in neonatal and adult rat retina. Neurosci Lett. 1995; 183:96-99.
23. Jelsma TN, Friedman HH, Berkelaar M, Bray GM, Aguayo AJ. Different forms of the neurotrophin receptor trkB mRNA predominate in rat retina and optic nerve. J Neurobiol. 1993;24:1207-1214.
24. Rodríguez-Tébar A, Dechant G, Götz R, Barde Y-A. Binding of neurotrophin-3 to its neuronal receptors and interaction with nerve growth factor and brain-derived neurotrophic factor. Eur Mol Biol Org J. 1989a; 11:917-922.
25. Rodríguez-Tebar A, Jeffrey PL, Thonen H, Barde Y-A. The survival of chick retinal ganglion cells in response to brain-derived neurotrophic factor depends on their embryonic age. Dev Biol. 1989b;136:296-303.
26. Johnson JE, Barde Y-A, Schwab M, Thoenen H. Brain derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells. J Neurosci. 1986;6:3031-3038.
27. Thanos S, Bähr M, Barde Y-A, Vanselow J. Survival and elongation of adult rat retinal ganglion cells: In vitro effects of lesioned sciatic nerve and brain derived neurotrophic factor. Eur J Neurosci. 1989;1:9-26.
28. Weibel D, Cadelli D, Schwab ME. Regeneration of lesioned rat optic nerve fibers is improved after neutralization of myelin-associated neurite growth inhibitors. Brain Res. 1994;642:259-266.
29. 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.
30. 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 USA. 1994;91:1632-1636.
31. Rodríguez-Tébar A, De la Rosa EJ, Arribas A. Neurotrophin-3 receptors in the developing chick retina. Eur J Biochem. 1993;211:789-794.
32. Lamballe F, Klein R, Barbacid M. Trk C, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell. 1991;66:967-971.
33. Escandon E, Soppet D, Rosenthal A, et al. Regulation of neurotrophin receptor expression during embryonic and postnatal development. J Neurosci. 1994;14:2054-2068.
34. Peinado-Ramón P, Salvador M, Vidal-Sanz M. In vivo effects of the administration of the neurotrophins BDNF and NT-3 on the survival of injured adult rat retinal ganglion cells. Eur J Physiol. 1994; 427(1,suppl):50. Abstract.
35. Peinado-Ramón P, Salvador M, Vidal-Sanz M. In vivo effects of the administration of the neurotrophins BDNF and NT-3 on the survival of injured adult rat retinal ganglion cells. ARVO Abstracts. Invest Ophthalmol Vis Sci. 1995;36:S4205.
36. Vidal-Sanz M, Villegas-Pérez MP, Bray GM, Aguayo AJ. Persistent retrograde labelling of adult rat retinal ganglion cells with the carbocyanine dye dil. Exp Neural. 1988; 102:92-101.
37. Linden R, Perry VH. Massive retinotectal projection in rats. Brain Res. 1983;272:145-149.
38. Martin PR. The projection of different retinal ganglion cell classes to the dorsal geniculate nucleus in the hooded rat. Exp Brain Res. 1986;62:77-88.
39. Schmued LC, Fallon JH. Fluoro-gold: A new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res. 1986;377:147-154.
40. Vidal-Sanz M, Bray GM, Villegas-Pérez MP, Thanos S, Aguayo AJ. Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J Neurosci. 1987;7:2894-2909.
41. Vidal-Sanz M, Bray GM, Aguayo AJ. Regenerated synapses persist in the superior colliculus after the re-growth of retinal ganglion cell axons. J Neurocytol. 1991;20:40-952.
42. Vidal-Sanz M, Villegas-Pérez MP, Bray GM, Aguayo AJ. Use of peripheral nerve grafts to study regeneration after CNS injury. Neuroprotocols. 1993;3:29-33.
43. Ip NY, Stitt TN, Tapley P, et al. Similarities and differences in the way neurotrophins interact with the trk receptors in neuronal and non-neuronal cells. Neuron. 1993;10:137-149.
44. Dodd J, Solter D, Jessell TM. Monoclonal antibodies against carbohydrate differentiation antigens identify subsets of primary sensory neurones. Nature. 1984;311:469-472.
45. Thanos S. The relationship of microglial cells to dying neurons during natural neuronal cell death and axotomy-induced degeneration of the rat retina. Eur J Neurosci. 1991;3:1189-1207.
46. Thanos S, Pavlidis C, Mey J, Thiel HJ. Specific transcellular staining of microglia in the adult rat after traumatic degeneration of carbocynine-filled retinal ganglion cells. Exp Eye Res. 1992;54:377-391.
47. 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.
48. Perry VH, Henderson Z, Linden R. Postnatal changes in retinal ganglion cells and optic axon populations in the pigmented rat. J Comp Neurol. 1983;219:356-368.
49. Vidal-Sanz M, Sellés I, Salvador M, Villegas-Pérez MP. Quantitative studies on retinal ganglion cell death after transient periods of ischaemia. ARVO Abstracts. Invest Ophthalmol Vis Sci. 1994;35:82087.
50. Berkelaar M, Clarke DB, Wang Y-C, Bray GM, Aguayo AJ. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci. 1994;14:4368-4374.
51. Perry VH. Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience. 1981;6:931-944.
52. Thanos S. Alterations in the morphology of ganglion cell dendrites in the adult rat retina after optic nerve transection and grafting of peripheral nerve segments. Cell Tissue Res. 1988;254:599-609.
53. Vidal-Sanz M, Sellés I, Salvador M, Villegas-Pérez MP. Short and long term effects of transient periods of ischemia on retinal ganglion cell death: A quantitative in vivo study. ARVO Abstracts. Invest Ophthalmol Vis Sci. 1995;36:S4295.
54. García-Valenzuela E, Gorczyca W, Darzynkiewicz Z, Sharma SC. Apoptosis in adult rat retinal ganglion cells after axotomy. J Neurobiol. 1994;25:431-438.
55. Quigley HA, Nickells RW, Kerrigan LA, Pease ME, Thibault DJ, Zack DJ. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774-786.
56. Rabacchi SA, Bonfanti L, Liu X-H, Maffei L. Apoptotic cell death induced by optic nerve lesion in the neonatal rat. J Neurosci. 1994;14:5292-5301.
57. De la Rosa EJ, Arribas A, Frade JM, Rodríguez-Tébar A. Role of neurotrophins in the control of neural development: Neurotrophin-3 promotes both neuron differentiation and survival of cultured chick retinal cells. Neuroscience. 1994;58:347-352.
58. Okazawa H, Kamei M, Kazanawa I. Molecular cloning and expression of a novel truncated form of chicken trkC. FEBS Lett. 1993;329:171-177.
59. Okazawa H, Nishiyama K, Kamei M, et al. Trk immunoreactivity at neuronal dendrite and cell body. Biochem Biophys Res Comm. 1994;194:683-690.
60. Friedman WJ, Ernfors P, Persson H. Transient and persistent expression of NT-3/HDNF mRNA in the rat brain during postnatal development. J Neurosci. 1991;11:1577-1584.
61. Kittlerova P, Playford DE, Bray GM, Aguayo AJ. NT-3 enhances growth and upregulates GAP43 in a subset of retinal ganglion cells after axotomy. Soc Neurosci Abstr. 1994;20(part 2):1098.
62. Soppet D, Escandon E, Maragos J, et al. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell. 1991;65:895-903.
63. LNGFR in NT-4 signalling. EMBO J. 1995;14:1979-1990.
64. Carmignoto G, Maffei L, Candeo P, Canella R, Comelli MC. Effect of NGF on the survival of rat retinal ganglion cells following optic nerve section. J Neurosci. 1989;9:1263-1272.
65. Sievers J, Hausmann B, Unsicker K, Berry M. Fibroblast growth factors promote the survival of adult retinal ganglion cells after transection of the optic nerve. Neurosci Lett. 1987;76:157-162.
66. Thanos S, Mey J. Type-specific stabilization and target-dependent survival of regenerating ganglion cells in the retina of adult rats. J Neurosci. 1995;15:1057-1079.