The mechanism of axonal degeneration after perikaryal excitotoxic injury to the retina

Experimental Neurology

Volumn 236, Issue 1, 2012, Pages 34-45

  Bull, Natalie D ^a   Chidlow, Glyn ^b,c   Wood, John P M ^b,c   Martin, Keith R ^a,b,d   Casson, Robert J ^b,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c HANSON INSTITUTE   (Australia)

^d UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Excitotoxicity; Neurodegeneration; Wallerian

Indexed keywords

HLA ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL SURVIVAL; CONTROLLED STUDY; DISEASE ASSOCIATION; EXCITOTOXICITY; IMMUNOHISTOCHEMISTRY; LYMPHOCYTIC INFILTRATION; MICROGLIA; NERVE CELL LESION; NERVE FIBER DEGENERATION; NONHUMAN; PERIKARYAL EXITOTOXIC RENAL GANGLION CELL INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RETINA NERVE CELL; WILD TYPE;

ANIMALS; AXONS; DISEASE MODELS, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RETINAL DEGENERATION; RETINAL GANGLION CELLS; WALLERIAN DEGENERATION;

EID: 84861716388     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.03.021     Document Type: Article

References (40)

1. Adalbert R., Gillingwater T.H., Haley J.E., Bridge K., Beirowski B., Berek L., Wagner D., Grumme D., Thomson D., Celik A., Addicks K., Ribchester R.R., Coleman M.P. A rat model of slow Wallerian degeneration (WldS) with improved preservation of neuromuscular synapses. Eur. J. Neurosci. 2005, 21:271-277.
2. Adalbert R., Nogradi A., Szabo A., Coleman M.P. The slow Wallerian degeneration gene in vivo protects motor axons but not their cell bodies after avulsion and neonatal axotomy. Eur. J. Neurosci. 2006, 24:2163-2168.
3. Beirowski B., Adalbert R., Wagner D., Grumme D.S., Addicks K., Ribchester R.R., Coleman M.P. The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci. 2005, 6:6.
4. Beirowski B., Babetto E., Coleman M.P., Martin K.R. The WldS gene delays axonal but not somatic degeneration in a rat glaucoma model. Eur. J. Neurosci. 2008, 28:1166-1179.
5. Beirowski B., Nogradi A., Babetto E., Garcia-Alias G., Coleman M.P. Mechanisms of axonal spheroid formation in central nervous system Wallerian degeneration. J. Neuropathol. Exp. Neurol. 2010, 69:455-472.
6. Bosco A., Steele M.R., Vetter M.L. Early microglia activation in a mouse model of chronic glaucoma. J. Comp. Neurol. 2011, 519:599-620.
7. Brandstatter J.H., Hartveit E., Sassoe-Pognetto M., Wassle H. Expression of NMDA and high-affinity kainate receptor subunit mRNAs in the adult rat retina. Eur. J. Neurosci. 1994, 6:1100-1112.
8. Brown M.C., Lunn E.R., Perry V.H. Consequences of slow Wallerian degeneration for regenerating motor and sensory axons. J. Neurobiol. 1992, 23:521-536.
9. 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.
10. Bull N.D., Irvine K.A., Franklin R.J., Martin K.R. Transplanted oligodendrocyte precursor cells reduce neurodegeneration in a model of glaucoma. Invest. Ophthalmol. Vis. Sci. 2009, 50:4244-4253.
11. Casson R.J. Possible role of excitotoxicity in the pathogenesis of glaucoma. Clin. Experiment. Ophthalmol. 2006, 34:54-63.
12. Chen S., Bisby M.A. Impaired motor axon regeneration in the C57BL/Ola mouse. J. Comp. Neurol. 1993, 333:449-454.
13. Chidlow G., Wood J.P., Manavis J., Osborne N.N., Casson R.J. Expression of osteopontin in the rat retina: effects of excitotoxic and ischemic injuries. Invest. Ophthalmol. Vis. Sci. 2008, 49:762-771.
14. Chidlow G., Wood J.P., Sarvestani G., Manavis J., Casson R.J. Evaluation of Fluoro-Jade C as a marker of degenerating neurons in the rat retina and optic nerve. Exp. Eye Res. 2009, 88:426-437.
15. Chidlow G., Ebneter A., Wood J.P., Casson R.J. The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma. Acta Neuropathol. (Berl) 2011, 121:737-751.
16. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
17. Doble A. The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol. Ther. 1999, 81:163-221.
18. Ebneter A., Casson R.J., Wood J.P., Chidlow G. Microglial activation in the visual pathway in experimental glaucoma: spatiotemporal characterization and correlation with axonal injury. Invest. Ophthalmol. Vis. Sci. 2010, 51:6448-6460.
19. Ebneter A., Chidlow G., Wood J.P., Casson R.J. Protection of retinal ganglion cells and the optic nerve during short-term hyperglycemia in experimental glaucoma. Arch. Ophthalmol. 2011, 129:1337-1344.
20. Fischer L.R., Culver D.G., Tennant P., Davis A.A., Wang M., Castellano-Sanchez A., Khan J., Polak M.A., Glass J.D. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 2004, 185:232-240.
21. George E.B., Glass J.D., Griffin J.W. Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J. Neurosci. 1995, 15:6445-6452.
22. Gilley J., Coleman M.P. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 2010, 8:e1000300.
23. Hanisch U.K., Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007, 10:1387-1394.
24. Howell G.R., Libby R.T., Jakobs T.C., Smith R.S., Phalan F.C., Barter J.W., Barbay J.M., Marchant J.K., Mahesh N., Porciatti V., Whitmore A.V., Masland R.H., John S.W. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 2007, 179:1523-1537.
25. Hynd M.R., Scott H.L., Dodd P.R. Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease. Neurochem. Int. 2004, 45:583-595.
26. Ito D., Tanaka K., Suzuki S., Dembo T., Fukuuchi Y. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 2001, 32:1208-1215.
27. Johnson T.V., Bull N.D., Hunt D.P., Marina N., Tomarev S.I., Martin K.R. Neuroprotective effects of intravitreal mesenchymal stem cell transplantation in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2010, 51:2051-2059.
28. Karadottir R., Cavelier P., Bergersen L.H., Attwell D. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 2005, 438:1162-1166.
29. Mack T.G., Reiner M., Beirowski B., Mi W., Emanuelli M., Wagner D., Thomson D., Gillingwater T., Court F., Conforti L., Fernando F.S., Tarlton A., Andressen C., Addicks K., Magni G., Ribchester R.R., Perry V.H., Coleman M.P. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 2001, 4:1199-1206.
30. Matute C., Alberdi E., Domercq M., Sanchez-Gomez M.V., Perez-Samartin A., Rodriguez-Antiguedad A., Perez-Cerda F. Excitotoxic damage to white matter. J. Anat. 2007, 210:693-702.
31. Meller D., Eysel U.T., Schmidt-Kastner R. Transient immunohistochemical labelling of rat retinal axons during Wallerian degeneration by a monoclonal antibody to neurofilaments. Brain Res. 1994, 648:162-166.
32. Perry V.H., Brown M.C., Lunn E.R. Very slow retrograde and Wallerian degeneration in the CNS of C57BL/Ola mice. Eur. J. Neurosci. 1991, 3:102-105.
33. Ruifrok A.C., Johnston D.A. Quantification of histochemical staining by color deconvolution. Anal. Quant. Cytol. Histol. 2001, 23:291-299.
34. Saggu S.K., Chotaliya H.P., Cai Z., Blumbergs P., Casson R.J. The spatiotemporal pattern of somal and axonal pathology after perikaryal excitotoxic injury to retinal ganglion cells: a histological and morphometric study. Exp. Neurol. 2008, 211:52-58.
35. Saggu S.K., Chotaliya H.P., Blumbergs P.C., Casson R.J. Wallerian-like axonal degeneration in the optic nerve after excitotoxic retinal insult: an ultrastructural study. BMC Neurosci. 2010, 11:97.
36. Stokin G.B., Lillo C., Falzone T.L., Brusch R.G., Rockenstein E., Mount S.L., Raman R., Davies P., Masliah E., Williams D.S., Goldstein L.S. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005, 307:1282-1288.
37. van den Hoorn T., Paul P., Jongsma M.L., Neefjes J. Routes to manipulate MHC class II antigen presentation. Curr. Opin. Immunol. 2011, 23:88-95.
38. Walter L., Neumann H. Role of microglia in neuronal degeneration and regeneration. Semin. Immunopathol. 2009, 31:513-525.
39. Wang A.L., Yuan M., Neufeld A.H. Degeneration of neuronal cell bodies following axonal injury in Wld(S) mice. J. Neurosci. Res. 2006, 84:1799-1807.
40. Zhai Q., Wang J., Kim A., Liu Q., Watts R., Hoopfer E., Mitchison T., Luo L., He Z. Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 2003, 39:217-225.