Early interneuron dysfunction in ALS: Insights from a mutant sod1 zebrafish model

Annals of Neurology

Volumn 73, Issue 2, 2013, Pages 246-258

  McGown, Alexander ^a   McDearmid, Jonathan R ^b   Panagiotaki, Niki ^a   Tong, Huaxia ^b   Al Mashhadi, Sufana ^a   Redhead, Natasha ^a   Lyon, Alison N ^c   Beattie, Christine E ^c   Shaw, Pamela J ^a,d   Ramesh, Tennore M ^a,d  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c OHIO STATE UNIVERSITY   (United States)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APOMORPHINE; COPPER ZINC SUPEROXIDE DISMUTASE; MUTANT PROTEIN; RILUZOLE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STRESS; CONTROLLED STUDY; INTERNEURON; MOTONEURON; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ZEBRA FISH;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOMORPHINE; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; GENES, REPORTER; GLYCINE; HSP72 HEAT-SHOCK PROTEINS; HUMANS; INTERNEURONS; MICE; MOTOR NEURONS; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; PATCH-CLAMP TECHNIQUES; RILUZOLE; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84884213153     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23780     Document Type: Article

References (47)

1. Jucker M, Walker LC,. Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 2011; 70: 532-540.
2. Turner BJ, Talbot K,. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol 2008; 85: 94-134.
3. Bosco DA, Morfini G, Karabacak NM, et al. Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat Neurosci 2010; 13: 1396-1403.
4. Guareschi S, Cova E, Cereda C, et al. An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1. Proc Natl Acad Sci U S A 2012; 109: 5074-5079.
5. Polymenidou M, Cleveland DW,. The seeds of neurodegeneration: prion-like spreading in ALS. Cell 2011; 147: 498-508.
6. Couthouis J, Hart MP, Shorter J, et al. A yeast functional screen predicts new candidate ALS disease genes. Proc Natl Acad Sci U S A 2011; 108: 20881-20890.
7. Shaw BF, Valentine JS,. How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends Biochem Sci 2007; 32: 78-85.
8. Ferraiuolo L, Kirby J, Grierson AJ, et al. Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat Rev Neurol 2011; 7: 616-630.
9. Dion PA, Daoud H, Rouleau GA,. Genetics of motor neuron disorders: new insights into pathogenic mechanisms. Nat Rev Genet 2009; 10: 769-782.
10. Armon C,. From clues to mechanisms: understanding ALS initiation and spread. Neurology 2008; 71: 872-873.
11. Verstraete E, van den Heuvel MP, Veldink JH, et al. Motor network degeneration in amyotrophic lateral sclerosis: a structural and functional connectivity study. PLoS One 2010; 5: e13664.
12. Ravits JM, La Spada AR,. ALS motor phenotype heterogeneity, focality, and spread: deconstructing motor neuron degeneration. Neurology 2009; 73: 805-811.
13. Ramesh T, Lyon AN, Pineda RH, et al. A genetic model of amyotrophic lateral sclerosis in zebrafish displays phenotypic hallmarks of motoneuron disease. Dis Model Mech 2010; 3: 652-662.
14. Friedrich RW, Jacobson GA, Zhu P,. Circuit neuroscience in zebrafish. Curr Biol 2010; 20: R371-R381.
15. Tyedmers J, Mogk A, Bukau B,. Cellular strategies for controlling protein aggregation. Nat Rev Mol Cell Biol 2010; 11: 777-788.
16. Drapeau P, Ali DW, Buss RR, Saint-Amant L,. In vivo recording from identifiable neurons of the locomotor network in the developing zebrafish. J Neurosci Methods 1999; 88: 1-13.
17. Lea R, Bonev B, Dubaissi E, et al. Multiple fluorescent in situ mRNA hybridization (FISH) on whole mounts and sections. In:, Hoppler S, Vize PD, eds. Xenopus protocols. 2nd ed. New York, NY: Human Press, 2012.
18. Batista MF, Lewis KE,. Pax2/8 act redundantly to specify glycinergic and GABAergic fates of multiple spinal interneurons. Dev Biol 2008; 323: 88-97.
19. Costes SV, Daelemans D, Cho EH, et al. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 2004; 86: 3993-4003.
20. Li Q, Lau A, Morris TJ, et al. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 2004; 24: 4070-4081.
21. Hao le T, Burghes AH, Beattie CE,. Generation and characterization of a genetic zebrafish model of SMA carrying the human SMN2 gene. Mol Neurodegener 2011; 6: 24.
22. Gidalevitz T, Prahlad V, Morimoto RI,. The stress of protein misfolding: From single cells to multicellular organisms. Cold Spring Harb Perspect Biol. 2011; 3 (6)
23. Lewis KE, Eisen JS,. From cells to circuits: development of the zebrafish spinal cord. Prog Neurobiol 2003; 69: 419-449.
24. Higashijima S, Schaefer M, Fetcho JR,. Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish. J Comp Neurol 2004; 480: 19-37.
25. Goulding M,. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 2009; 10: 507-518.
26. McLean DL, Fan J, Higashijima S, et al. A topographic map of recruitment in spinal cord. Nature 2007; 446: 71-75.
27. Carrasco DI, Bichler EK, Seburn KL, Pinter MJ,. Nerve terminal degeneration is independent of muscle fiber genotype in SOD1 mice. PLoS One 2010; 5: e9802.
28. Dupuis L, Pradat PF, Ludolph AC, Loeffler JP,. Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurol 2011; 10: 75-82.
29. Wong M, Martin LJ,. Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Hum Mol Genet 2010; 19: 2284-2302.
30. Bai CX, Glaaser IW, Sawanobori T, Sunami A,. Involvement of local anesthetic binding sites on IVS6 of sodium channels in fast and slow inactivation. Neurosci Lett 2003; 337: 41-45.
31. Riley BE, Kaiser SE, Kopito RR,. Autophagy inhibition engages Nrf2-p62 Ub-associated signaling. Autophagy 2011; 7: 338-340.
32. Riley BE, Kaiser SE, Shaler TA, et al. Ubiquitin accumulation in autophagy-deficient mice is dependent on the Nrf2-mediated stress response pathway: a potential role for protein aggregation in autophagic substrate selection. J Cell Biol 2010; 191: 537-552.
33. Hara H, Ohta M, Adachi T,. Apomorphine protects against 6-hydroxydopamine-induced neuronal cell death through activation of the Nrf2-ARE pathway. J Neurosci Res 2006; 84: 860-866.
34. Turner MR, Kiernan MC,. Does interneuronal dysfunction contribute to neurodegeneration in amyotrophic lateral sclerosis? Amyotroph Lateral Scler 2012; 13: 245-250.
35. Durand J, Amendola J, Bories C, Lamotte d'Incamps B,. Early abnormalities in transgenic mouse models of amyotrophic lateral sclerosis. J Physiol Paris 2006; 99: 211-220.
36. Martin LJ, Chang Q,. Inhibitory synaptic regulation of motoneurons: a new target of disease mechanisms in amyotrophic lateral sclerosis. Mol Neurobiol 2012; 45: 30-42.
37. Raynor EM, Shefner JM,. Recurrent inhibition is decreased in patients with amyotrophic lateral sclerosis. Neurology 1994; 44: 2148-2153.
38. Vucic S, Nicholson GA, Kiernan MC,. Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain 2008; 131 (pt 6): 1540-1550.
39. Chang Q, Martin LJ,. Glycine receptor channels in spinal motoneurons are abnormal in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurosci 2011; 31: 2815-2827.
40. Weber M, Eisen A, Stewart HG, Andersen PM,. Preserved slow conducting corticomotoneuronal projections in amyotrophic lateral sclerosis with autosomal recessive D90A CuZn-superoxide dismutase mutation. Brain 2000; 123 (pt 7): 1505-1515.
41. Hossaini M, Cardona Cano S, van Dis V, et al. Spinal inhibitory interneuron pathology follows motor neuron degeneration independent of glial mutant superoxide dismutase 1 expression in SOD1-ALS mice. J Neuropathol Exp Neurol 2011; 70: 662-677.
42. Pambo-Pambo A, Durand J, Gueritaud JP,. Early excitability changes in lumbar motoneurons of transgenic SOD1G85R and SOD1G(93A-Low) mice. J Neurophysiol 2009; 102: 3627-3642.
43. Dal Canto MC, Gurney ME,. 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 1995; 676: 25-40.
44. Jaarsma D, Haasdijk ED, Grashorn JA, et al. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis 2000; 7 (6 pt B): 623-643.
45. Gould TW, Buss RR, Vinsant S, et al. Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J Neurosci 2006; 26: 8774-8786.
46. Murray LM, Talbot K, Gillingwater TH,. Review: Neuromuscular synaptic vulnerability in motor neurone disease: amyotrophic lateral sclerosis and spinal muscular atrophy. Neuropathol Appl Neurobiol 2010; 36: 133-156.
47. Doble A,. The pharmacology and mechanism of action of riluzole. Neurology 1996; 47 (6 suppl 4): S233-S241.