Time-course of the retinal nerve fibre layer degeneration after complete intra-orbital optic nerve transection or crush: A comparative study

Vision Research

Volumn 49, Issue 23, 2009, Pages 2808-2825

  Parrilla Reverter, Guillermo ^a,b   Agudo, Marta ^a,b   Nadal Nicolás, Francisco ^a   Alarcón Martínez, Luis ^a   Jiménez López, Manuel ^a   Salinas Navarro, Manuel ^a   Sobrado Calvo, Paloma ^a   Bernal Garro, José M ^a   Villegas Pérez, María P ^a   Vidal Sanz, Manuel ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

Author keywords

Neurofilament; Neuronal degeneration; Optic nerve injury; Retina; Retinal ganglion cell

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITE; FEMALE; IMAGE ANALYSIS; IMMUNOHISTOLOGY; NERVE FIBER DEGENERATION; NERVE TRANSECTION; NEUROFILAMENT; NONHUMAN; OPTIC NERVE INJURY; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RAT; RETINA DEGENERATION; RETINA GANGLION CELL; RETINA NERVE CELL; SPRAGUE DAWLEY RAT;

ANIMALS; AXONS; DISEASE PROGRESSION; FEMALE; NERVE CRUSH; NERVE FIBERS; NEUROFILAMENT PROTEINS; OPTIC NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; RETINAL DEGENERATION; RETINAL GANGLION CELLS;

EID: 70449530860     PISSN: 00426989     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.visres.2009.08.020     Document Type: Article

References (75)

1. Agudo M., Pérez-Marín M., Lönngren U., Sobrado P., Conesa A., Cánovas I., et al. Time course profiling of the retinal transcriptome after optic nerve transection and optic nerve crush. Molecular Vision 14 (2008) 1050-1063
2. Agudo M., Pérez-Marín M.C., Sobrado-Calvo P., Lonngren U., Salinas-Navarro M., Canovas I., et al. Immediate upregulation of proteins belonging to different branches of the apoptotic cascade in the retina after optic nerve transection and optic nerve crush. Investigative Ophthalmology and Visual Science 50 (2009) 424-431
3. Al Chalabi A., and Miller C.C. Neurofilaments and neurological disease. BioEssays 25 (2003) 346-355
4. Anderton B.H., Breinburg D., Downes M.J., Green P.J., Tomlinson B.E., Ulrich J., et al. Monoclonal antibodies show that neurofibrillary tangles and neurofilaments share antigenic determinants. Nature 298 (1982) 84-86
5. Avilés-Trigueros M., Mayor-Torroglosa S., García-Avilés A., Lafuente M.P., Rodríguez M.E., Miralles de Imperial J., et al. Transient ischemia of the retina results in massive degeneration of the retinotectalprojection: Long-term neuroprotection with brimonidine. Experimental Neurology 184 2 (2003) 767-777
6. Aviles-Trigueros M., Sauve Y., Lund R.D., and Vidal-Sanz M. Selective innervation of retinorecipient brainstem nuclei by retinal ganglion cell axons regenerating through peripheral nerve grafts in adult rats. Journal of Neuroscience 20 (2000) 361-374
7. Bahr M., Eschweiler G.W., and Wolburg H. Precrushed sciatic nerve grafts enhance the survival and axonal regrowth of retinal ganglion cells in adult rats. Experimental Neurology 116 (1992) 13-22
8. Balkema G.W., and Drager U.C. Light-dependent antibody labelling of photoreceptors. Nature 316 (1985) 630-633
9. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., and Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. Journal of Neuroscience 14 (1994) 4368-4374
10. Buckingham B.P., Inman D.M., Lambert W., Oglesby E., Calkins D.J., Steele M.R., et al. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. Journal of Neuroscience 28 (2008) 2735-2744
11. Burke W., Cottee L.J., Garvey J., Kumarasinghe R., and Kyriacou C. Selective degeneration of optic nerve fibres in the cat produced by a pressure block. Journal of Physiology 376 (1986) 461-476
12. Cairns N.J., Atkinson P.F., Hanger D.P., Anderton B.H., Daniel S.E., and Lantos P.L. Tau protein in the glial cytoplasmic inclusions of multiple system atrophy can be distinguished from abnormal tau in Alzheimer's disease. Neuroscience Letters 230 (1997) 49-52
13. Chidlow G., Casson R., Sobrado-Calvo P., Vidal-Sanz M., and Osborne N.N. Measurement of retinal injury in the rat after optic nerve transection: An RT-PCR study. Molecular Vision 11 (2005) 387-396
14. Cho E.Y., and So K.F. Regrowth of retinal ganglion cell axons into a peripheral nerve graft in the adult hamster is enhanced by a concurrent optic nerve crush. Experimental Brain Research 78 (1989) 567-574
15. Coleman M.P., and Anderton B.H. Phosphate-dependent monoclonal antibodies to neurofilaments and Alzheimer neurofibrillary tangles recognize a synthetic phosphopeptide. Journal of Neurochemistry 54 (1990) 1548-1555
16. Dieterich D.C., Trivedi N., Engelmann R., Gundelfinger E.D., Gordon-Weeks P.R., and Kreutz M.R. Partial regeneration and long-term survival of rat retinal ganglion cells after optic nerve crush is accompanied by altered expression, phosphorylation and distribution of cytoskeletal proteins. European Journal of Neuroscience 15 (2002) 1433-1443
17. Drager U.C., and Hofbauer A. Antibodies to heavy neurofilament subunit detect a subpopulation of damaged ganglion cells in retina. Nature 309 (1984) 624-626
18. Gotow T., Tanaka J., and Takeda M. The organization of neurofilaments accumulated in perikaryon following aluminum administration: Relationship between structure and phosphorylation of neurofilaments. Neuroscience 64 (1995) 553-569
19. Hoffman P.N., Cleveland D.W., Griffin J.W., Landes P.W., Cowan N.J., and Price D.L. Neurofilament gene expression: A major determinant of axonal caliber. Proceedings of the National Academy of Sciences of the United States of America 84 (1987) 3472-3476
20. Hoffman P.N., Pollock S.C., and Striph G.G. Altered gene expression after optic nerve transection: Reduced neurofilament expression as a general response to axonal injury. Experimental Neurology 119 (1993) 32-36
21. Johnstone M., Goold R.G., Fischer I., and Gordon-Weeks P.R. The neurofilament antibody RT97 recognises a developmentally regulated phosphorylation epitope on microtubule-associated protein 1B. Journal of Anatomy 191 Pt 2 (1997) 229-244
22. Ksiezak-Reding H., Dickson D.W., Davies P., and Yen S.H. Recognition of tau epitopes by anti-neurofilament antibodies that bind to Alzheimer neurofibrillary tangles. Proceedings of the National Academy of Sciences of the United States of America 84 (1987) 3410-3414
23. Lafuente Lopez-Herrera M.P., Mayor-Torroglosa S., Miralles d I., Villegas-Pérez M.P., and Vidal-Sanz M. Transient ischemia of the retina results in altered retrograde axoplasmic transport: Neuroprotection with brimonidine. Experimental Neurology 178 (2002) 243-258
24. Lafuente M.P., Villegas-Pérez M.P., Mayor S., Aguilera M.E., Miralles de Imperial J., and Vidal-Sanz M. Neuroprotective effects of brimonidine against transientischemia-induced retinal ganglion cell death: A dose response in vivo study. Experimental Eye Research 74 2 (2002) 181-189
25. Lafuente M.P., Villegas-Pérez M.P., Selles-Navarro I., Mayor-Torroglosa S., Miralles d I., and Vidal-Sanz M. Retinal ganglion cell death after acute retinal ischemia is an ongoing process whose severity and duration depends on the duration of the insult. Neuroscience 109 (2002) 157-168
26. Leoz y Arcuate J. Procesos regenerativos del nervio óptico y retina, con ocasión de injertos nerviosos. Trab del lab de Invest Biol (1914)
27. Lewis S.E., and Nixon R.A. Multiple phosphorylated variants of the high molecular mass subunit of neurofilaments in axons of retinal cell neurons: Characterization and evidence for their differential association with stationary and moving neurofilaments. Journal of Cell Biology 107 (1988) 2689-2701
28. Lindqvist N., Peinado-Ramon P., Vidal-Sanz M., and Hallbook F. GDNF, Ret, GFRalpha1 and 2 in the adult rat retino-tectal system after optic nerve transection. Experimental Neurology 187 (2004) 487-499
29. Lindqvist N., Vidal-Sanz M., and Hallbook F. Single cell RT-PCR analysis of tyrosine kinase receptor expression in adult rat retinal ganglion cells isolated by retinal sandwiching. Brain Research Protocols 10 (2002) 75-83
30. Mansour-Robaey S., Clarke D.B., Wang Y.C., Bray G.M., and 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 91 5 (1994) 1632-1636 Mar1
31. Marco-Gomariz M.A., Hurtado-Montalban N., Vidal-Sanz M., Lund R.D., and Villegas-Pérez M.P. Phototoxic-induced photoreceptor degeneration causes retinal ganglion cell degeneration in pigmented rats. Journal of Comparative Neurology 498 (2006) 163-179
32. Mayor-Torroglosa S., De l V., Rodriguez M.E., Lopez-Herrera M.P., Aviles-Trigueros M., Garcia-Avilés A., et al. Ischemia results 3 months later in altered ERG, degeneration of inner layers, and deafferented tectum: Neuroprotection with brimonidine. Investigative Ophthalmology and Visual Science 46 (2005) 3825-3835
33. McKerracher L., Essagian C., and Aguayo A.J. Temporal changes in beta-tubulin and neurofilament mRNA levels after transection of adult rat retinal ganglion cell axons in the optic nerve. Journal of Neuroscience 13 (1993) 2617-2626
34. McKerracher L., Vidal-Sanz M., and Aguayo A.J. Slow transport rates of cytoskeletal proteins change during regeneration of axotomized retinal neurons in adult rats. Journal of Neuroscience 10 (1990) 641-648
35. McKerracher L., Vidal-Sanz M., Essagian C., and Aguayo A.J. Selective impairment of slow axonal transport after optic nerve injury in adult rats. Journal of Neuroscience 10 (1990) 2834-2841
36. Morrison J.C., Johnson E.C., Cepurna W.O., and Funk R.H. Microvasculature of the rat optic nerve head. Investigative Ophthalmology and Visual Science 40 (1999) 1702-1709
37. Nadal-Nicolás F.M., Jiménez-López M., Sobrado-Calvo P., Nieto-López L., Canovas-Martinez I., Salinas-Navarro M., et al. Brn3a as a marker of retinal ganglion cells: Qualitative and quantitative time course studies in naïve and optic nerve injured retinas. Investigative Ophthalmology Visual Science 50 8 (2009) 3860-3868
38. Nixon R.A., Lewis S.E., Dahl D., Marotta C.A., and Drager U.C. Early posttranslational modifications of the three neurofilament subunits in mouse retinal ganglion cells: Neuronal sites and time course in relation to subunit polymerization and axonal transport. Brain Research. Molecular Brain Research 5 (1989) 93-108
39. Parrilla-Reverter G., Agudo M., Sobrado-Calvo P., Salinas-Navarro M., Villegas-Pérez M.P., and Vidal-Sanz M. Effects of different neurotrophic factors on the survival of retinal ganglion cells after a complete intraorbital nerve crush injury: A quantitative in vivo study. Experimental Eye Research 89 1 (2009) 32-41
40. Parrilla-Reverter, G., Sobrado Calvo, P., Cánovas Martínez, I., Bernal Garro, J. M., Soro, M. I., Aguilera Meseguer, M. E., et al. (2006). Retinal ganglion cell axotomy induced by intraorbital nerve crush or optic nerve transection results in different time course degeneration and expression of neurofilaments. Investigative Ophthalmology and Visual Science, 47. E-Abstract 1248.
41. Peinado-Ramon P., Salvador M., Villegas-Pérez M.P., and 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 and Visual Science 37 (1996) 489-500
42. Perrot R., Berges R., Bocquet A., and Eyer J. Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration. Molecular Neurobiology 38 (2008) 27-65
43. Petzold A. Neurofilament phosphoforms: Surrogate markers for axonal injury, degeneration and loss. Journal of the Neurological Sciences 233 (2005) 183-198
44. Ramón y Cajal, S. (1914). Estudios sobre la degeneración y regeneración del sistema nervioso. In: Hijos de Nicolás, M. Moya (Eds.), Tomo II (pp. 203-217).
45. Robinson G.A. Immediate early gene expression in axotomized and regenerating retinal ganglion cells of the adult rat. Brain Research. Molecular Brain Research 24 (1994) 43-54
46. Salinas-Navarro, M., Alarcón-Martínez, L., Valiente-Soriano, F.J., Jiménez-López, M., Mayor-Torroglosa, S., & Avilés-Trigueros, M., et al. (submitted for publication). Ocular hypertension impairs optic nerve axonal transport leading to progressive retinal ganglion cell degeneration. Experimental Eye Research.
47. Salinas-Navarro M., Jiménez-López M., Valiente-Soriano F., Alarcón-Martínez L., Aviles-Trigueros M., Mayor-Torroglosa S., et al. Retinal ganglion cell population in adult albino and pigmented mice: A computerised analysis of the entire population and its spatial distribution. Vision Research 49 (2009) 647-673
48. Salinas-Navarro M., Mayor-Torroglosa S., Jiménez-López M., Aviles-Trigueros M., Holmes T.M., Lund R.D., et al. A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vision Research 49 (2009) 115-126
49. Salinas-Navarro M., Napankangas U., Turunen J., Veijola F., Valiente-Soriano F., Villegas-Pérez M.P., et al. Effects of acute increase of intraocular pressure in adult pigmented rats: Assessment of the retinal nerve fiber layer (in vivo) and the retinal ganglion cell population. Investigative Ophthalmology and Visual Science 9 (2008) 90-99 E-Abstract 5480
50. Salvador-Silva M., Vidal-Sanz M., and Villegas-Pérez M.P. Microglial cells in theretina of Carassius auratus: Effects of optic nerve crush. Journal of Comparative Neurology 417 4 (2000) 431-447 Feb 21
51. Sasaki H., Coffey P., Villegas-Pérez M.P., Vidal-Sanz M., Young M.J., Lund R.D., et al. Light induced EEG desynchronization and behavioral arousal in rats with restored retinocollicular projection by peripheral nerve graft. Neuroscience Letters 218 (1996) 45-48
52. Silveira L.C., Russelakis-Carneiro M., and Perry V.H. The ganglion cell response to optic nerve injury in the cat: Differential responses revealed by neurofibrillar staining. Journal of Neurocytology 23 2 (1994) 75-86 Feb
53. Sobrado-Calvo P., Vidal-Sanz M., and Villegas-Pérez M.P. Rat retinal microglial cells under normal conditions, after optic nerve section, and after optic nerve section and intravitreal injection of trophic factors or macrophage inhibitory factor. Journal of Comparative Neurology 501 (2007) 866-878
54. Soto I., Oglesby E., Buckingham B.P., Son J.L., Roberson E.D., Steele M.R., et al. Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. Journal of Neuroscience 28 (2008) 548-561
55. Sternberger N.H., Sternberger L.A., and Ulrich J. Aberrant neurofilament phosphorylation in Alzheimer disease. Proceedings of the National Academy of Sciences of the United States of America 82 (1985) 4274-4276
56. Tello, F. (1907). La régénération dans les voies optiques. In: Trabajos de Laboratorio en Investigación Biológica (pp. 237-248).
57. Thanos S., and Vanselow J. Adult retinal ganglion cells retain the ability to regenerate their axons up to several weeks after axotomy. Journal of Neuroscience Research 22 (1989) 144-149
58. Veeranna, Lee J.H., Pareek T.K., Jaffee H., Boland B., Vinod K.Y., et al. Neurofilament tail phosphorylation: Identity of the RT97 phosphoepitope and regulation in neurons by cross-talk among proline-directed kinases. Journal of Neurochemistry 107 (2008) 35-49
59. Vidal-Sanz M., Aviles-Trigueros M., Whiteley S.J., Sauve Y., and Lund R.D. Reinnervation of the pretectum in adult rats by regenerated retinal ganglion cell axons: Anatomical and functional studies. Peripheral and Spinal Mechanisms in the Neural Control of Movement 137 (2002) 443-452
60. Vidal-Sanz M., Bray G.M., and Aguayo A.J. Regenerated synapses persist in the superior colliculus after the regrowth of retinal ganglion cell axons. Journal of Neurocytology 20 (1991) 940-952
61. Vidal-Sanz M., Bray G.M., Villegas-Pérez M.P., Thanos S., and Aguayo A.J. Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. Journal of Neuroscience 7 (1987) 2894-2909
62. Vidal-Sanz M., De la Villa P., Aviles-Trigueros M., Mayor-Torroglosa S., Salinas-Navarro M., Alarcón-Martínez L., et al. Neuroprotection of retinal ganglion cell function and their central nervous system targets. Eye 21 (2007) S42-S45
63. Vidal-Sanz M., Lafuente M.P., Mayor S., de Imperial J.M., and Villegas-Pérez M.P. Retinal ganglion cell death induced by retinal ischemia neuroprotective effects of two alpha-2 agonists. Survey of Ophthalmology 45 Suppl. 3 (2001) S261-S267
64. Vidal-Sanz M., Villegas-Pérez M.P., Bray G.M., and Aguayo A.J. Use of peripheral nerve grafts to study regeneration after CNS injury. Neuroprotocols 3 (1993) 29-33
65. Villegas-Pérez M.P., Lawrence J.M., Vidal-Sanz M., Lavail M.M., and Lund R.D. Ganglion cell loss in RCS rat retina: A result of compression of axons by contracting intraretinal vessels linked to the pigment epithelium. Journal of Comparative Neurology 392 (1998) 58-77
66. Villegas-Pérez M.P., Vidal-Sanz M., Bray G.M., and Aguayo A.J. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. Journal of Neuroscience 8 (1988) 265-280
67. Villegas-Pérez M.P., Vidal-Sanz M., and Lund R.D. Mechanism of retinal ganglion cell loss in inherited retinal dystrophy. NeuroReport 7 (1996) 1995-1999
68. Villegas-Pérez M.P., Vidal-Sanz M., Rasminsky M., Bray G.M., and Aguayo A.J. Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. Journal of Neurobiology (1993) 24 23-36
69. Wang S., Villegas-Pérez M.P., Holmes T., Lawrence J.M., Vidal-Sanz M., Hurtado-Montalban N., et al. Evolving neurovascular relationships in the RCS rat with age. Current Eye Research 27 (2003) 183-196
70. Wang S., Villegas-Pérez M.P., Vidal-Sanz M., and Lund R.D. Progressive optic axon dystrophy and vacuslar changes in rd mice. Investigative Ophthalmology and Visual Science 41 (2000) 537-545
71. Watanabe M., Sawai H., and Fukuda Y. Axonal regeneration of retinal ganglion cells in the cat geniculocortical pathway. Brain Research 560 (1991) 330-333
72. Whiteley S.J., Sauve Y., Aviles-Trigueros M., Vidal-Sanz M., and Lund R.D. Extent and duration of recovered pupillary light reflex following retinal ganglion cell axon regeneration through peripheral nerve grafts directed to the pretectum in adult rats. Experimental Neurology 154 (1998) 560-572
73. WoldeMussie E., Ruiz G., Wijono M., and Wheeler L.A. Neuroprotection of retinal ganglion cells by brimonidine in rats with laser-induced chronic ocular hypertension. Investigative Ophthalmology and Visual Science 42 (2001) 2849-2855
74. Wood J.N., and Anderton B.H. Monoclonal antibodies to mammalian neurofilaments. Bioscience Reports 1 (1981) 263-268
75. Yoles E., and Schwartz M. Degeneration of spared axons following partial white matter lesion: Implications for optic nerve neuropathies. Experimental Neurology 153 (1998) 1-7