Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF

Nature Neuroscience

Volumn 9, Issue 3, 2006, Pages 408-419

  Pun, San ^a   Santos, Alexandre Ferrão ^a   Saxena, Smita ^a   Xu, Lan ^a   Caroni, Pico ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HINDLIMB; MOTOR NEURON DISEASE; MOUSE; MUSCLE INNERVATION; NERVE FIBER; NEUROFILAMENT; NONHUMAN; PREDICTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REINNERVATION; TOPOGRAPHY;

ANIMALS; AXONS; CILIARY NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICE; MICE, TRANSGENIC; MOTOR NEURON DISEASE; MOTOR NEURONS; MUSCLE FATIGUE; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MUTATION; NERVE DEGENERATION; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; SUPEROXIDE DISMUTASE; SYNAPTIC VESICLES;

EID: 33344462702     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1653     Document Type: Article

References (50)

1. Coleman, P.D. & Yao, P.J. Synaptic slaughter in Alzheimer's disease. Neurobiol. Aging 24, 1023-1027 (2003).
2. Gurney, M.E. et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775 (1994).
3. Bruijn, L.I., Miller, T.M. & Cleveland, D.W. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723-749 (2004).
4. Frey, D. et al. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci. 20, 2534-2542 (2000).
5. Fischer, L.R. et al. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 185, 232-240 (2004).
6. Lino, M.M., Schneider, C. & Caroni, P. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J. Neurosci. 22, 4825-4832 (2002).
7. Clement, A.M. et al. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302, 113-117 (2003).
8. Liu, J. et al. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43, 5-17 (2004).
9. Pasinelli, P. et al. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 43, 19-30 (2004).
10. Wong, P.C. et al. An adverse property of a familial ALS-linked SOD1 mutation causes motoneuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14, 1105-1116 (1995).
11. Collard, J.F., Cote, F. & Julien, J.P. Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375, 61-64 (1995).
12. Zhang, B., Tu, P., Abtahian, F., Trojanowski, J.Q. & Lee, V.M. Neurofilaments and orthograde transport are reduced in ventral root axons of transgenic mice that express human SOD1 with a G93A mutation. J. Cell Biol. 139, 1307-1315 (1997).
13. Williamson, T.L. & Cleveland, D.W. Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat. Neurosci. 2, 50-56 (1999).
14. Pinter, M.J., Waldeck, R.F., Wallace, N. & Crok, L.C. Motor unit behavior in canine motor neuron disease. J. Neurosci. 15, 3447-3457 (1995).
15. Kostic, V., Jackson-Lewis, V., de Bilbao, F., Dubois-Dauphin, M. & Przedborski, S. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 277, 559-562 (1997).
16. Sagot, Y. et al. Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease. J. Neurosci. 15, 7727-7733 (1995).
17. Lobsiger, C.S., Garcia, M.L., Ward, C.M. & Cleveland, D.W. Altered axonal architecture by removal of the heavily phosphorylated neurofilament tail domains strongly slows superoxide dismutase 1 mutant-mediated ALS. Proc. Natl. Acad. Sci. USA 102, 10351-10356 (2005).
18. Sagot, Y., Rosse, T., Vejsada, R., Perrelet, D. & Kato, A.C. Differential effects of neurotrophic factors on motoneuron retrograde labeling in a murine model of motoneuron disease. J. Neurosci. 18, 1132-1141 (1998).
19. Burke, R.E. Physiology of motor units. in Myology (eds. Engel, A.G. & Franzini-Armstrong, C.) 464-484 (McGraw-Hill, New York, 1994).
20. De Paola, V., Arber, S. & Caroni, P. AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks. Nat. Neurosci. 6, 491-500 (2003).
21. Stokin, G.B. et al. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307, 1282-1288 (2005).
22. Gunawardena, S. & Goldstein, L.S. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch. Neurol. 62, 46-51 (2005).
23. Nguyen, Q.T., Sanes, J.R. & Lichtman, J.W. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5, 861-867 (2002).
24. Watts, R.J., Hoopfer, E.D. & Luo, L. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38, 871-885 (2003).
25. Zhai, Q. et al. Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 39, 217-225 (2003).
26. Raff, M.C., Whitmore, A.V. & Finn, J.T. Axonal self-destruction and neurodegeneration. Science 296, 868-871 (2002).
27. Bruijn, L.I. et al. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18, 327-338 (1997).
28. Bommel, H. et al. Missense mutation in the tubulin-specific chaperone E (Tbce) gene in the mouse mutant progressive motor neuronopathy, a model of human motoneuron disease. J. Cell Biol. 159, 563-569 (2002).
29. Williamson, T.L. et al. Absence of neurofilaments reduces the selective vulnerability of motor neurons and slows disease caused by a familial amyotrophic lateral sclerosis-linked superoxide dismutase 1 mutant. Proc. Natl. Acad. Sci. USA 95, 9631-9636 (1998).
30. Couillard-Despres, S. et al. Protective effect of neurofilament heavy gene overexpression in motor neuron disease induced by mutant superoxide dismutase. Proc. Natl. Acad. Sci. USA 95, 9626-9630 (1998).
31. Peterson, W.M., Wang, Q., Tzekova, R. & Wiegand, S.J. Ciliary neurotrophic factor and stress stimuli activate the Jak-STAT pathway in retinal neurons and glia. J. Neurosci. 20, 4081-4090 (2000).
32. Park, K., Luo, J.M., Hisheh, S., Harvey, A.R. & Cui, Q. Cellular mechanisms associated with spontaneous and ciliary neurotrophic factor-cAMP-induced survival and axonal regeneration of adult retinal ganglion cells. J. Neurosci. 24, 10806-10815 (2004).
33. Lee, H.H., Dadgostar, H., Cheng, Q., Shu, J. & Cheng, G. NF-kappaB-mediated upregulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. USA 96, 9136-9141 (1999).
34. Delio, D.A., Fiori, M.G. & Lowndes, H.E. Motor unit function during evolution of proximal axon swellings. J. Neurol. Sci. 109, 30-40 (1992).
35. LaMonte, B.H. et al. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34, 715-727 (2002).
36. Xia, C.H. et al. Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J. Cell Biol. 161, 55-66 (2003).
37. Al-Chalabi, A. et al. Ciliary neurotrophic factor genotype does not influence clinical phenotype in amyotrophic lateral sclerosis. Ann. Neurol. 54, 130-134 (2003).
38. Giess, R. et al. Early onset of severe familial amyotrophic lateral sclerosis with a SOD-1 mutation: potential impact of CNTF as a candidate modifier gene. Am. J. Hum. Genet. 70, 1277-1286 (2002).
39. Schaefer, A.M., Sanes, J.R. & Lichtman, J.W. A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J. Comp. Neurol. 490, 209-219 (2005).
40. Atkin, J.D. et al. Properties of slow- and fast-twitch muscle fibres in a mouse model of amyotrophic lateral sclerosis. Neuromuscul. Disord. 15, 377-388 (2005).
41. Raoul, C, (2002) Motoneuron death triggered by a specific pathway downstream of Fas: potentiation by ALS-linked SOD1 mutations. Neuron 35, 1067-1083 (2002).
42. Dengler, R. et al. Amyotrophic lateral sclerosis: macro-EMG and twitch forces of single motor units. Muscle Nerve 13, 545-550 (1990).
43. Larsson, L., Li, X., Tollback, A. & Grimby, L. Contractile properties in single muscle fibers from chronically overused motor units in relation to motoneuron firing properties in prior polio patients. J. Neurol. Sci. 132, 182-192 (1995).
44. Nguyen, M.D., Lariviere, R.C. & Julien, J.P. Reduction of axonal caliber does not alleviate motor neuron disease caused by mutant superoxide dismutase 1. Proc. Natl. Acad. Sci. USA 97, 12306-12311 (2000).
45. Shaw, P.J. & Eggett, C.J. Molecular factors underlying selective vulnerability of motor neurons to neurodegeneration in amyotrophic lateral sclerosis. J. Neurol. 247, I17-I27 (2000).
46. von Lewinski, F. & Keller, B.U. Ca2+, mitochondria and selective motoneuron vulnerability: implications for ALS. Trends Neurosci. 28, 494-500 (2005).
47. Kuo, J.J. et al. Hyperexcitability of cultured spinal motoneurons from presymptomatic ALS mice. J. Neurophysiol. 91, 571-575 (2004).
48. Gunawardena, S. & Goldstein, L.S. Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32, 389-401 (2001).
49. Gunawardena, S. et al. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40, 25-40 (2003).
50. Mittoux, V. et al. Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease. Hum. Gene Ther. 11, 1177-1187 (2000).