Characterization of intercostal muscle pathology in canine degenerative myelopathy: A disease model for amyotrophic lateral sclerosis

Journal of Neuroscience Research

Volumn 91, Issue 12, 2013, Pages 1639-1650

  Morgan, Brandie R ^a   Coates, Joan R ^b   Johnson, Gayle C ^b   Bujnak, Alyssa C ^a   Katz, Martin L ^a  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Disease model; Dog; Morphometry; Neurodegeneration; SOD1

Indexed keywords

CHOLINERGIC RECEPTOR; COPPER ZINC SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE MODEL; EXPERIMENTAL DOG; GENOTYPE; HISTOPATHOLOGY; INTERCOSTAL MUSCLE; MOTONEURON; NEUROMUSCULAR SYNAPSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD ATROPHY; TISSUE CHARACTERIZATION;

DISEASE MODEL; DOG; MORPHOMETRY; NEURODEGENERATION; SOD1;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; DOGS; HUMANS; INTERCOSTAL MUSCLES; MUTATION, MISSENSE; SPINAL CORD DISEASES; SUPEROXIDE DISMUTASE;

EID: 84886641380     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23287     Document Type: Article

References (33)

1. Acevedo-Arozena A, Kalmar B, Essa S, Ricketts T, Joyce P, Kent R, Rowe C, Parker A, Gray A, Hafezparast M, Thorpe JR, Greensmith L, Fisher EM. 2011. A comprehensive assessment of the SOD1G93A low-copy transgenic mouse, which models human amyotrophic lateral sclerosis. Dis Models Mech 4:686-700.
2. Al-Chalabi A, Andersen PM, Chioza B, Shaw C, Sham PC, Robberecht W, Matthijs G, Camu W, Marklund SL, Forsgren L, Rouleau G, Laing NG, Hurse PV, Siddique T, Leigh PN, Powell JF. 1998. Recessive amyotrophic lateral sclerosis families with the D90A SOD1 mutation share a common founder: evidence for a linked protective factor. Hum Mol Genet 7:2045-2050.
3. Al-Chalabi A, Jones A, Troakes C, King A, Al-Sarraj S, van den Berg LH. 2012. The genetics and neuropathology of amyotrophic lateral sclerosis. Acta Neuropathol 124:339-352.
4. Andersen PM, Nilsson P, Ala-Hurula V, Keranen ML, Tarvainen I, Haltia T, Nilsson L, Binzer M, Forsgren L, Marklund SL. 1995. Amyotrophic lateral sclerosis associated with homozygosity for an Asp90Ala mutation in CuZn-superoxide dismutase. Nat Genet 10:61-66.
5. Andersen PM, Forsgren L, Binzer M, Nilsson P, Ala-Hurula V, Keranen ML, Bergmark L, Saarinen A, Haltia T, Tarvainen I, Kinnunen E, Udd B, Marklund SL. 1996. Autosomal recessive adult-onset amyotrophic lateral sclerosis associated with homozygosity for Asp90Ala CuZn-superoxide dismutase mutation. A clinical and genealogical study of 36 patients. Brain 119:1153-1172.
6. Armstrong RB, Saubert CW, Seeherman HJ, Taylor CR. 1982. Distribution of fiber types in locomotory muscles of dogs. Am J Anat 163:87-98.
7. Averill DR Jr. 1973. Degenerative myelopathy in the aging German shepherd dog: clinical and pathologic findings. J Am Vet Med Assoc 162:1045-1051.
8. Awano T, Johnson GS, Wade CM, Katz ML, Johnson GC, Taylor JF, Perloski M, Biagi T, Baranowska I, Long S, March PA, Olby NJ, Shelton GD, Khan S, O'Brien DP, Lindblad-Toh K, Coates JR. 2009. Genome-wide association analysis reveals a SOD1 mutation in canine degenerative myelopathy that resembles amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 106:2794-2799.
9. Baloh RH, Rakowicz W, Gardner R, Pestronk A. 2007. Frequent atrophic groups with mixed-type myofibers is distinctive to motor neuron syndromes. Muscle Nerve 36:107-110.
10. Bassel-Duby R, Olson EN. 2006. Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75:19-37.
11. Braund KG, McGuire JA, Lincoln CE. 1982. Observations on normal skeletal muscle of mature dogs: a cytochemical, histochemical, and morphometric study. Vet Pathol 19:577-595.
12. Brooks BR, Miller RG, Swash M, Munsat TL. 2000. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293-299.
13. Charcot J-M. 1869. Deuxcas d'atrophie musculaire progressive avec lesions del substance grise et de faisceaux anterolateraux de moelle epiniere. Arch Physiol Norm Pathol:354-357.
14. Coates JR, Wininger FA. 2010. Canine degenerative myelopathy. Vet Clin North Am Small Anim Pract 40:929-950.
15. Coates JR, March PA, Oglesbee M, Ruaux CG, Olby NJ, Berghaus RD, O'Brien DP, Keating JH, Johnson GS, Williams DA. 2007. Clinical characterization of a familial degenerative myelopathy in Pembroke Welsh corgi dogs. J Vet Intern Med 21:1323-1331.
16. Dadon-Nachum M, Melamed E, Offen D. 2011. The "dying-back" phenomenon of motor neurons in ALS. J Mol Neurosci 43:470-477.
17. de Carvalho M, Pinto S, Swash M. 2010. Association of paraspinal and diaphragm denervation in ALS. Amyotroph Lateral Scler 11:63-66.
18. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD. 2004. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185:232-240.
19. Fischer LR, Brotherton T, Glass JD. 2013. Axonal degeneration in the peripheral nervous system: Implications for the pathogenesis of amyotrophic lateral sclerosis. Exp Neurol (in press).
20. 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.
21. Griffiths IR, Duncan ID. 1975. Chronic degenerative radiculomyelopathy in the dog. J Small Anim Pract 16:461-471.
22. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, et al. 1994. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772-1775.
23. Hegedus J, Putman CT, Gordon T. 2007. Time course of preferential motor unit loss in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 28:154-164.
24. Khoris J, Moulard B, Briolotti V, Hayer M, Durieux A, Clavelou P, Malafosse A, Rouleau GA, Camu W. 2000. Coexistence of dominant and recessive familial amyotrophic lateral sclerosis with the D90A Cu, Zn superoxide dismutase mutation within the same country. Eur J Neurol 7:207-211.
25. Lobsiger CS, Garcia ML, Ward CM, Cleveland DW. 2005. Altered axonal architecture by removal of the heavily phosphorylated neurofilament tail domains strongly slows superoxide dismutase 1 mutant-mediated ALS. Proc Natl Acad Sci U S A 102:10351-10356.
26. March PA, Coates JR, Abyad RJ, Williams DA, O'Brien DP, Olby NJ, Keating JH, Oglesbee M. 2009. Degenerative myelopathy in 18 Pembroke Welsh corgi dogs. Vet Pathol 46:241-250.
27. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, et al. 1993. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62.
28. Schaefer AM, Sanes JR, Lichtman JW. 2005. A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J Comp Neurol 490:209-219.
29. Shelton GD, Johnson GC, O'Brien DP, Katz ML, Pesayco JP, Chang BJ, Mizisin AP, Coates JR. 2012. Degenerative myelopathy associated with a missense mutation in the superoxide dismutase 1 (SOD1) gene progresses to peripheral neuropathy in Pembroke Welsh corgis and boxers. J Neurol Sci 318:55-64.
30. Shen H, Barry DM, Dale JM, Garcia VB, Calcutt NA, Garcia ML. 2011. Muscle pathology without severe nerve pathology in a new mouse model of Charcot-Marie-Tooth disease type 2E. Hum Mol Genet 20:2535-2548.
31. Simmons BJ, Cohen TJ, Bedlack R, Yao TP. 2011. HDACs in skeletal muscle remodeling and neuromuscular disease. Hdbk Exp Pharmacol 206:79-101.
32. Soraru G, D'Ascenzo C, Nicolao P, Volpe M, Martignago S, Palmieri A, Romeo V, Koutsikos K, Piccione F, Cima V, Pegoraro E, Angelini C. 2008. Muscle histopathology in upper motor neuron-dominant amyotrophic lateral sclerosis. Amyotroph Lateral Scler 9:287-293.
33. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, Sisodia SS, Cleveland DW, Price DL. 1995. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14:1105-1116.