Degeneration of axons in spinal white matter in G93A mSOD1 mouse characterized by NFL and alpha-internexin immunoreactivity

Brain Research

Volumn 1465, Issue , 2012, Pages 90-100

  King, Anna E ^a   Blizzard, Catherine A ^a   Southam, Katherine A ^a   Vickers, James C ^a   Dickson, Tracey C ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

ALS; Axon degeneration; Neuronal intermediate filament; Spinal cord

Indexed keywords

ALPHA INTERNEXIN; GREEN FLUORESCENT PROTEIN; MUTANT PROTEIN; NEUROFILAMENT PROTEIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE FIBER; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; SPINAL CORD ATROPHY; WESTERN BLOTTING; WHITE MATTER;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONS; DISEASE MODELS, ANIMAL; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR NEURONS; NERVE DEGENERATION; NEUROFILAMENT PROTEINS; SPINAL CORD; SPINAL CORD DISEASES; SUPEROXIDE DISMUTASE;

ANIMALIA; MUS;

EID: 84862866928     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.05.018     Document Type: Article

References (47)

1. Abe, A., Numakura, C., Saito, K., Koide, H., Oka, N., Honma, A., Kishikawa, Y., Hayasaka, K., 2009. Neurofilament light chain polypeptide gene mutations in Charcot-Marie-Tooth disease: nonsense mutation probably causes a recessive phenotype. J. Hum. Genet. 54, 94-97.
2. Bareyre, F.M., Kerschensteiner, M., Misgeld, T., Sanes, J.R., 2005. Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury. Nat. Med. 11, 1355-1360. (Pubitemid 41752918)
3. Browne, S.E., Yang, L., DiMauro, J.P., Fuller, S.W., Licata, S.C., Beal, M.F., 2006. Bioenergetic abnormalities in discrete cerebral motor pathways presage spinal cord pathology in the G93A SOD1 mouse model of ALS. Neurobiol. Dis. 22, 599-610. (Pubitemid 43832131)
4. Cairns, N.J., Uryu, K., Bigio, E.H., Mackenzie, I.R., Gearing, M., Duyckaerts, C., Yokoo, H., Nakazato, Y., Jaros, E., Perry, R.H., Arnold, S.E., Lee, V.M., Trojanowski, J.Q., 2004. alpha-Internexin aggregates are abundant in neuronal intermediate filament inclusion disease (NIFID) but rare in other neurodegenerative diseases. Acta Neuropathol. (Berl) 108, 213-223. (Pubitemid 39199513)
5. Cavanagh, J.B., 1964. The significance of the "dying back" process in experimental and human neurological disease. Int. Rev. Exp. Pathol. 3, 219-267.
6. Chien, C.L., Mason, C.A., Liem, R.K., 1996. alpha-Internexin is the only neuronal intermediate filament expressed in developing cerebellar granule neurons. J. Neurobiol. 29, 304-318. (Pubitemid 26071973)
7. Chiu, F.C., Barnes, E.A., Das, K., Haley, J., Socolow, P., Macaluso, F.P., Fant, J., 1989. Characterization of a novel 66 kd subunit of mammalian neurofilaments. Neuron 2, 1435-1445.
8. Chou, S.M., Norris, F.H., 1993. Amyotrophic lateral sclerosis: lower motor neuron disease spreading to upper motor neurons. Muscle Nerve 16, 864-869. (Pubitemid 23209146)
9. Chung, Y.H., Joo, K.M., Nam, R.H., Cho, M.H., Kim, D.J., Lee, W.B., Cha, C.I., 2005. Decreased expression of calretinin in the cerebral cortex and hippocampus of SOD1G93A transgenic mice. Brain Res. 1035, 105-109. (Pubitemid 40248543)
10. Cowin, G.J., Butler, T.J., Kurniawan, N.D., Watson, C., Wallace, R.H., 2011. Magnetic resonance microimaging of the spinal cord in the SOD1 mouse model of amyotrophic lateral sclerosis detects motor nerve root degeneration. NeuroImage 58, 69-74.
11. Dal Canto, M.C., Gurney, M.E., 1994. Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am. J. Pathol. 145, 1271-1279. (Pubitemid 24378480)
12. Dal Canto, M.C., Gurney, M.E., 1995. Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu, Zn SOD, and in mice overexpressing wild type human SOD: a model of familial amyotrophic lateral sclerosis (FALS). Brain Res. 676, 25-40.
13. Deng, H.X., Zhai, H., Fu, R., Shi, Y., Gorrie, G.H., Yang, Y., Liu, E., Dal Canto, M.C., Mugnaini, E., Siddique, T., 2007. Distal axonopathy in an alsin-deficient mouse model. Hum. Mol. Genet. 16, 2911-2920. (Pubitemid 350048388)
14. Dickson, T.C., King, C.E., McCormack, G.H., Vickers, J.C., 1999. Neurochemical diversity of dystrophic neurites in the early and late stages of Alzheimer's disease. Exp. Neurol. 156 (1), 100-110. (Pubitemid 29152987)
15. Dickson, T.C., Chuckowree, J.A., Chuah, M.I., West, A.K., Vickers, J.C., 2005. alpha-Internexin immunoreactivity reflects variable neuronal vulnerability in Alzheimer's disease and supports the role of the beta-amyloid plaques in inducing neuronal injury. Neurobiol. Dis. 18, 286-295. (Pubitemid 40431112)
16. Feng, G., Mellor, R.H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M., Nerbonne, J.M., Lichtman, J.W., Sanes, J.R., 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51.
17. Fischer, L.R., Culver, D.G., Tennant, P., Davis, A.A., Wang, M., Castellano-Sanchez, A., Khan, J., Polak, M.A., Glass, J.D., 2004. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 185, 232-240. (Pubitemid 38084849)
18. Frey, D., Schneider, C., Xu, L., Borg, J., Spooren, W., Caroni, P., 2000. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci. 20, 2534-2542. (Pubitemid 30220340)
19. Guo, Y.S., Wu, D.X., Wu, H.R., Wu, S.Y., Yang, C., Li, B., Bu, H., Zhang, Y.S., Li, C.Y., 2009. Sensory involvement in the SOD1-G93A mouse model of amyotrophic lateral sclerosis. Exp. Mol. Med. 41, 140-150.
20. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.X., et al., 1994. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264, 1772-1775. (Pubitemid 24227760)
21. Imai, T., Minami, R., Nagaoka, M., Ishikawa, Y., Kameda, K., Okabe, M., Matsumoto, H., 1990. Proximal and distal motor nerve conduction velocities in Werdnig-Hoffmann disease. Pediatr. Neurol. 6, 82-86. (Pubitemid 20268464)
22. Kaplan, M.P., Chin, S.S., Fliegner, K.H., Liem, R.K., 1990. Alpha-internexin, a novel neuronal intermediate filament protein, precedes the low molecular weight neurofilament protein (NF-L) in the developing rat brain. J. Neurosci. 10, 2735-2748.
23. Kassa, R.M., Mariotti, R., Bonaconsa, M., Bertini, G., Bentivoglio, M., 2009. Gene, cell, and axon changes in the familial amyotrophic lateral sclerosis mouse sensorimotor cortex. J. Neuropathol. Exp. Neurol. 68, 59-72.
24. King, A.E., Dickson, T.C., Blizzard, C.A., Foster, S.S., Chung, R.S., West, A.K., Chuah, M.I., Vickers, J.C., 2007. Excitotoxicity mediated by non-NMDA receptors causes distal axonopathy in long-term cultured spinal motor neurons. Eur. J. Neurosci. 26, 2151-2159. (Pubitemid 47620492)
25. King, A.E., Dickson, T.C., Blizzard, C.A., Woodhouse, A., Foster, S.S., Chung, R.S., Vickers, J.C., 2011. Neuron-glia interactions underlie ALS-like axonal cytoskeletal pathology. Neurobiol. Aging 32, 459-469.
26. Leichsenring, A., Linnartz, B., Zhu, X.R., Lubbert, H., Stichel, C.C., 2006. Ascending neuropathology in the CNS of a mutant SOD1 mouse model of amyotrophic lateral sclerosis. Brain Res. 1096, 180-195. (Pubitemid 43928918)
27. Leigh, P.N., Swash, M., 1991. Cytoskeletal pathology in motor neuron diseases. Adv. Neurol. 56, 115-124.
28. Lennertz, R.C., Medler, K.A., Bain, J.L., Wright, D.E., Stucky, C.L., 2011. Impaired sensory nerve function and axon morphology in mice with diabetic neuropathy. J. Neurophysiol. 106 (2), 905-914.
29. Lin, W.L., Zehr, C., Lewis, J., Hutton, M., Yen, S.H., Dickson, D.W., 2005. Progressive white matter pathology in the spinal cord of transgenic mice expressing mutant (P301L) human tau. J. Neurocytol. 34, 397-410. (Pubitemid 44252072)
30. LoPachin, R.M., Ross, J.F., Lehning, E.J., 2002. Nerve terminals as the primary site of acrylamide action: a hypothesis. Neurotoxicology 23, 43-59. (Pubitemid 36559697)
31. Minciacchi, D., Kassa, R.M., Del Tongo, C., Mariotti, R., Bentivoglio, M., 2009. Voronoi- based spatial analysis reveals selective interneuron changes in the cortex of FALS mice. Exp. Neurol. 215, 77-86.
32. Morrison, B.M., Shu, I.W., Wilcox, A.L., Gordon, J.W., Morrison, J.H., 2000. Early and selective pathology of light chain neurofilament in the spinal cord and sciatic nerve of G86R mutant superoxide dismutase transgenic mice. Exp. Neurol. 165, 207-220.
33. Murray, L.M., Comley, L.H., Thomson, D., Parkinson, N., Talbot, K., Gillingwater, T.H., 2008. Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum. Mol. Genet. 17, 949-962. (Pubitemid 351426029)
34. Ozdinler, P.H., Benn, S., Yamamoto, T.H., Guzel, M., Brown Jr., R.H., Macklis, J.D., 2011. Corticospinal motor neurons and related subcerebral projection neurons undergo early and specific neurodegeneration in hSOD1G(3)A transgenic ALS mice. J. Neurosci. 31, 4166-4177.
35. Read, D.J., Li, Y., Chao, M.V., Cavanagh, J.B., Glynn, P., 2009. Neuropathy target esterase is required for adult vertebrate axon maintenance. J. Neurosci. 29, 11594-11600.
36. Read, D.J., Li, Y., Chao, M.V., Cavanagh, J.B., Glynn, P., 2010. Organophosphates induce distal axonal damage, but not brain oedema, by inactivating neuropathy target esterase. Toxicol. Appl. Pharmacol. 245 (1), 108-115.
37. Schaefer, A.M., Sanes, J.R., Lichtman, J.W., 2005. A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J. Comp. Neurol. 490, 209-219. (Pubitemid 41140989)
38. Schutz, B., Reimann, J., Dumitrescu-Ozimek, L., Kappes-Horn, K., Landreth, G.E., Schurmann, B., Zimmer, A., Heneka, M.T., 2005. The oral antidiabetic pioglitazone protects from neurodegeneration and amyotrophic lateral sclerosis-like symptoms in superoxide dismutase-G93A transgenic mice. J. Neurosci. 25, 7805-7812. (Pubitemid 41208652)
39. Soler-Martin, C., Vilardosa, U., Saldana-Ruiz, S., Garcia, N., Llorens, J., 2012. Loss of neurofilaments in the neuromuscular junction in a rat model of proximal axonopathy. Neuropathol. Appl. Neurobiol. 38 (1), 61-71.
40. Underwood, C.K., Kurniawan, N.D., Butler, T.J., Cowin, G.J., Wallace, R.H., 2011. Non-invasive diffusion tensor imaging detects white matter degeneration in the spinal cord of a mouse model of amyotrophic lateral sclerosis. NeuroImage 55, 455-461.
41. Volkening, K., Leystra-Lantz, C., Yang, W., Jaffee, H., Strong, M.J., 2009. Tar DNA binding protein of 43 kDa (TDP-43), 14-3-3 proteins and copper/zinc superoxide dismutase (SOD1) interact to modulate NFL mRNA stability. Implications for altered RNA processing in amyotrophic lateral sclerosis (ALS). Brain Res. 1305, 168-182.
42. Vucic, S., Cheah, B.C., Kiernan, M.C., 2009. Defining the mechanisms that underlie cortical hyperexcitability in amyotrophic lateral sclerosis. Exp. Neurol. 220, 177-182.
43. Watson, C.R., Paxinos, G., Kayalioglu, G., 2009. The Spinal Cord. Academic Press, San Diego.
44. Wong, N.K., He, B.P., Strong, M.J., 2000. Characterization of neuronal intermediate filament protein expression in cervical spinal motor neurons in sporadic amyotrophic lateral sclerosis (ALS). J. Neuropathol. Exp. Neurol. 59, 972-982.
45. Wood, J.D., Beaujeux, T.P., Shaw, P.J., 2003. Protein aggregation in motor neurone disorders. Neuropathol. Appl. Neurobiol. 29, 529-545. (Pubitemid 37548348)
46. Yuan, A., Rao, M.V., Sasaki, T., Chen, Y., Kumar, A., Veeranna, Liem, R.K., Eyer, J., Peterson, A.C., Julien, J.P., Nixon, R.A., 2006. Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS. J. Neurosci. 26, 10006-10019. (Pubitemid 44477162)
47. Zang, D.W., Cheema, S.S., 2002. Degeneration of corticospinal and bulbospinal systems in the superoxide dismutase 1(G93A G1H) transgenic mouse model of familial amyotrophic lateral sclerosis. Neurosci. Lett. 332, 99-102. (Pubitemid 35217850)