Spinocerebellar ataxia type 13 mutation that is associated with disease onset in infancy disrupts axonal pathfinding during neuronal development

DMM Disease Models and Mechanisms

Volumn 5, Issue 6, 2012, Pages 921-929

  Issa, Fadi A ^a   Mock, Allan F ^a   Sagasti, Alvaro ^b   Papazian, Diane M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL DEATH; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE ASSOCIATION; FERTILIZATION; GENE MUTATION; IMAGE RECONSTRUCTION; INFANCY; MOTONEURON; NERVE CELL DIFFERENTIATION; NERVE FIBER; NONHUMAN; ONSET AGE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPINAL CORD; SPINOCEREBELLAR ATAXIA TYPE 13; SPINOCEREBELLAR DEGENERATION; THREE DIMENSIONAL IMAGING; ZEBRA FISH;

AGE OF ONSET; AMINO ACID SUBSTITUTION; ANIMALS; AXONS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFANT; MICE; MODELS, NEUROLOGICAL; MOTOR NEURONS; MUTATION; NEUROGENESIS; SHAW POTASSIUM CHANNELS; SPINOCEREBELLAR DEGENERATIONS; SYNAPSES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84870009566     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.010157     Document Type: Article

References (34)

1. Brooke, R. E., Moores, T. S., Morris, N. P., Parson, S. H. and Deuchars, J. (2004). Kv3 voltage-gated potassium channels regulate neurotransmitter release from mouse motor nerve terminals. Eur. J. Neurosci. 20, 3313-3321.
2. Brooke, R. E., Atkinson, L., Edwards, I., Parson, S. H. and Deuchars, J. (2006). Immunohistochemical localization of the voltage-gated potassium ion channel Kv3.3 in the rat medulla oblongata and thoracic spinal cord. Brain Res. 1070, 101-115.
3. Chang, S. Y., Zagha, E., Kwon, E. S., Ozaita, A., Bobik, M., Martone, M. E., Ellisman, M. H., Heintz, N. and Rudy, B. (2007). Distribution of Kv3.3 potassium channel subunits in distinct neuronal populations of mouse brain. J. Comp. Neurol. 502, 953-972.
4. Eisen, J. S. (1994). Development of motoneuronal phenotype. Annu. Rev. Neurosci. 17, 1-30.
5. Eisen, J. S. and Melançon, E. (2001). Interactions with identified muscle cells break motoneuron equivalence in embryonic zebrafish. Nat. Neurosci. 4, 1065-1070.
6. Eisen, J. S., Myers, P. Z. and Westerfield, M. (1986). Pathway selection by growth cones of identified motoneurons in live zebrafish embryos. Nature 320, 269-271.
7. Eisen, J. S., Pike, S. H. and Debu, B. (1989). The growth cones of identified motoneurons in embryonic zebrafish select appropriate pathways in the absence of specific cellular interactions. Neuron 2, 1097-1104.
8. Eisen, J. S., Pike, S. H. and Romancier, B. (1990). An identified motoneuron with variable fates in embryonic zebrafish. J. Neurosci. 10, 34-43.
9. Figueroa, K. P., Minassian, N. A., Stevanin, G., Waters, M., Garibyan, V., Forlani, S., Strzelczyk, A., Bürk, K., Brice, A., Dürr, A. et al. (2010). KCNC3: Phenotype, mutations, channel biophysics - a study of 260 familial ataxia patients. Hum. Mutat. 31, 191-196.
10. Figueroa, K. P., Waters, M. F., Garibyan, V., Bird, T. D., Gomez, C. M., Ranum, L. P. W., Minassian, N. A., Papazian, D. M. and Pulst, S. M. (2011). Frequency of KCNC3 DNA variants as causes of spinocerebellar ataxia 13 (SCA13). PLoS ONE 6, e17811.
11. Flanagan-Steet, H., Fox, M. A., Meyer, D. and Sanes, J. R. (2005). Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132, 4471-4481.
12. Glaser, J. R. and Glaser, E. M. (1990). Neuron imaging with Neurolucida - a PC-based system for image combining microscopy. Comput. Med. Imaging Graph. 14, 307-317.
13. Hanson, M. G. and Landmesser, L. T. (2004). Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 43, 687-701.
14. Hanson, M. G. and Landmesser, L. T. (2006). Increasing the frequency of spontaneous rhythmic activity disrupts pool-specific axon fasciculation and pathfinding of embryonic spinal motoneurons. J. Neurosci. 26, 12769-12780.
15. Herman-Bert, A., Stevanin, G., Netter, J., Rascol, O., Brassat, D., Calvas, P., Camuzat, A., Yuan, Q., Schalling, M., Dürr, A. et al. (2000). Mapping of spinocerebellar ataxia 13 to chromosome 19q13.3-q13.4 in a family with autosomal dominant cerebellar ataxia and mental retardation. Am. J. Hum. Genet. 67, 229-235.
16. Issa, F. A., Mazzochi, C., Mock, A. F. and Papazian, D. M. (2011). Spinocerebellar ataxia type 13 mutant potassium channel alters neuronal excitability and causes locomotor deficits in zebrafish. J. Neurosci. 31, 6831-6841.
17. Liu, D. W. C. and Westerfield, M. (1990). The formation of terminal fields in the absence of competitive interactions among primary motoneurons in zebrafish. J. Neurosci. 10, 3947-3959.
18. Melançon, E., Liu, D. W. C., Westerfield, M. and Eisen, J. S. (1997). Pathfinding by identified zebrafish motoneurons in the absence of muscle pioneers. J. Neurosci. 17, 7796-7804.
19. Minassian, N. A., Lin, M. A. and Papazian, D. M. (2012). Altered Kv3.3 gating in early onset spinocerebellar ataxia type 13. J. Physiol. 590, 1599-1614.
20. Ming, G., Henley, J., Tessier-Lavigne, M., Song, H. and Poo, M. (2001). Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29, 441-452.
21. Mock, A. F., Richardson, J. L., Hsieh, J.-Y., Rinetti, G. and Papazian, D. M. (2010). Functional effects of spinocerebellar ataxia type 13 mutations are conserved in zebrafish Kv3. 3 channels. BMC Neurosci. 11, 99.
22. Moody, W. J. and Bosma, M. M. (2005). Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol. Rev. 85, 883-941.
23. Moreno, R. L. and Ribera, A. B. (2009). Zebrafish motor neuron subtypes differ electrically prior to axonal outgrowth. J. Neurophysiol. 102, 2477-2484.
24. Myers, P. Z., Eisen, J. S. and Westerfield, M. (1986). Development and axonal outgrowth of identified motoneurons in the zebrafish. J. Neurosci. 6, 2278-2289.
25. Nakano, T., Windrem, M., Zappavigna, V. and Goldman, S. A. (2005). Identification of a conserved 125 base-pair Hb9 enhancer that specifies gene expression to spinal motor neurons. Dev. Biol. 283, 474-485.
26. Oppenheim, R. W. (1991). Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
27. Panzer, J. A., Song, Y. and Balice-Gordon, R. J. (2006). In vivo imaging of preferential motor axon outgrowth and synaptogenesis at prepatterned acetylcholine receptor clusters in embryonic zebrafish skeletal muscle. J. Neurosci. 26, 934-947.
28. Pike, S. H. and Eisen, J. S. (1990). Identified primary motoneurons in embryonic zebrafish select appropriate pathways in the absence of other primary motoneurons. J. Neurosci. 10, 44-49.
29. + channels designed for high-frequency repetitive firing. Trends Neurosci. 24, 517-526.
30. Serra, H. G., Duvick, L., Zu, T., Carlson, K., Stevens, S., Jorgensen, N., Lysholm, A., Burright, E., Zoghbi, H. Y., Clark, H. B. et al. (2006). RORα-mediated Purkinje cell development determines disease severity in adult SCA1 mice. Cell 127, 697-708.
31. Spitzer, N. C. (2006). Electrical activity in early neuronal development. Nature 444, 707-712.
32. Waters, M. F., Minassian, N. A., Stevanin, G., Figueroa, K. P., Bannister, J. P. A., Nolte, D., Mock, A. F., Evidente, V. G., Fee, D., Müller, U. et al. (2006). Mutations in the voltage-gated potassium channel KCNC3 cause degenerative and developmental CNS phenotypes. Nat. Genet. 38, 447-451.
33. Wen, H. and Brehm, P. (2005). Paired motor neuron-muscle recordings in zebrafish test the receptor blockade model for shaping synaptic current. J. Neurosci. 25, 8104-8111.
34. Westerfield, M., McMurray, J. V. and Eisen, J. S. (1986). Identified motoneurons and their innervation of axial muscles in the zebrafish. J. Neurosci. 6, 2267-2277.