Characterization of early pathogenesis in the SOD1G93A mouse model of ALS: Part I, background and methods

Brain and Behavior

Volumn 3, Issue 4, 2013, Pages 335-350

  Vinsant, Sharon ^a   Mansfield, Carol ^a   Jimenez Moreno, Ramon ^a   Moore, Victoria Del Gaizo ^b   Yoshikawa, Masaaki ^a,e   Hampton, Thomas G ^c   Prevette, David ^a   Caress, James ^d   Oppenheim, Ronald W ^a   Milligan, Carol ^a  

^a Department of Neurobiology and Anatomy   (United States)

^b ELON UNIVERSITY   (United States)

^c Mouse Specifics Inc   (United States)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Axons; Cytoplasmic vacuoles; Glia; Mega mitochondria; Mitochondria; Motoneurons; Motor function; NMJs

Indexed keywords

AGE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HISTOPATHOLOGY; MOTONEURON; MOTOR DYSFUNCTION; MOTOR NEURON DISEASE; MOUSE; MUSCLE DENERVATION; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL;

EID: 84893464166     PISSN: None     EISSN: 21623279     Source Type: Journal    
DOI: 10.1002/brb3.143     Document Type: Article

References (113)

1. Aggarwal, A., and G. Nicholson. 2002. Detection of preclinical motor neurone loss in SOD1 mutation carriers using motor unit number estimation. J. Neurol. Neurosurg. Psychiatry 73:199-201.
2. Amendola, J., B. Verrier, P. Roubertoux, and J. Durand. 2004. Altered sensorimotor development in a transgenic mouse model of amyotrophic lateral sclerosis. Eur. J. Neurosci. 20:2822-2826.
3. Appel, S. H., W. Zhao, D. R. Beers, and J. S. Henkel. 2011. The microglial-motoneuron dialogue in ALS. Acta Myol. 30:4-8.
4. Barnéoud, P., J. Lolivier, D. J. Sanger, B. Scatton, and P. Moser. 1997. Quantitative motor assessment in fALS mice: a longitudinal study. Neuroreport 8:2861-2865.
5. Barrett, E. F., J. N. Barrett, and G. David. 2011. Mitochondria in motor nerve terminals: function in health and in mutant superoxide dismutase 1 mouse models of familial ALS. J. Bioenerg. Biomembr. 43:581-586. doi: 10.1007/s10863-011-9392-1.
6. Benatar, M. 2007. Lost in translation: treatment trials in the SOD1 mouse and in human ALS. Neurobiol. Dis. 26:1-13.
7. Bendotti, C., N. Calvaresi, L. Chiveri, A. Prelle, M. Moggio, M. Braga, et al. 2001. Early vacuolization and mitochondrial damage in motor neurons of fALS mice are not associated with apoptosis or with changes in cytochrome oxidase histochemical reactivity. J. Neurol. Sci. 191:25-33.
8. Bettini, N. L., T. S. Moores, B. Baxter, J. Deuchars, and S. H. Parson. 2007. Dynamic remodelling of synapses can occur in the absence of the parent cell body. BMC Neurosci. 8:79.
9. Boaro, S. N., J. C. Soares, and B. Jr König. 1998. Comparative structural analysis of neuromuscular junctions in mice at different ages. Ann. Anat. 180:173-179.
10. Bodian, D. 1964. AN electron-microscopic study of the monkey spinal cord. I. Fine structure of normal motor column. II. Effects of retrograde chromatolysis. III. Cytologic effects of mild and virulent poliovirus infection. Bull. Johns Hopkins Hosp. 114:13-119.
11. Bodian, D. 1966. Electron microscopy: two major synaptic types on spinal motoneurons. Science 151:1093-1094.
12. Bodian, D. 1970. An electron microscopic characterization of classes of synaptic vesicles by means of controlled aldehyde fixation. J. Cell Biol. 44:115-124.
13. Bodian, D. 1972. "Synaptic diversity and characterization by electron microscopy". Pp. 45-65 in G. D. Pappas, D. P. Purpura, eds. Structure and function of synapses. Raven Press, New York.
14. Boillée, S., and D. W. Cleveland. 2008. Revisiting oxidative damage in ALS: microglia, Nox, and mutant SOD1. J. Clin. Invest. 118:474-478. doi: 10.1172/JCI34613.
15. Boillée, S., K. Yamanaka, C. S. Lobsiger, N. G. Copeland, N. A. Jenkins, G. Kassiotis, et al. 2006a. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392.
16. Boillée, S., C. Vande Velde, and D. W. Cleveland. 2006b. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39-59.
17. Bradley, W. G., P. Good, C. G. Rasool, and L. S. Adelman. 1983. Morphometric and biochemical studies of peripheral nerves in amyotrophic lateral sclerosis. Ann. Neurol. 14:267-277.
18. Brown, D., J. Lydon, M. McLaughlin, A. Stuart-Tilley, R. Tyszkowski, and S. Alper. 1996. Antigen retrieval in cryostat tissue sections and cultured cells by treatment with sodium dodecyl sulfate (SDS). Histochem. Cell Biol. 105:261-267.
19. Bruijn, L. I., and M. Cudkowicz. 2006. Therapeutic targets for amyotrophic lateral sclerosis: current treatments and prospects for more effective therapies. Expert Rev. Neurother. 6:417-429.
20. Bruijn, L. I., T. M. Miller, and D. W. Cleveland. 2004. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27:23-49.
21. Brussee, V., F. Tardif, and J. P. Tremblay. 1997. Muscle fibers of mdx mice are more vulnerable to exercise than those of normal mice. Neuromuscul. Disord. 7:487-492.
22. Cheroni, C., M. Marino, M. Tortarolo, P. Veglianese, S. De Biasi, E. Fontana, et al. 2009. Functional alterations of the ubiquitin-proteasome system in motor neurons of a mouse model of familial amyotrophic lateral sclerosis. Hum. Mol. Genet. 18:82-96. doi: 10.1093/hmg/ddn319. Epub 29 September 2008.
23. Chiesa, R., P. Piccardo, S. Dossena, L. Nowoslawski, K. A. Roth, and B. Ghetti. 2005. Bax deletion prevents neuronal loss but not neurological symptoms in a transgenic model of inherited prion disease. Proc. Natl. Acad. Sci. USA 102:238-243.
24. Chu-Wang, I. W., and R. W. Oppenheim. 1978. Cell death of motoneurons in the chick embryo spinal cord. II. A quantitative and qualitative analysis of degeneration in the ventral root, including evidence for axon outgrowth and limb innervation prior to cell death. J. Comp. Neurol. 177:59-85.
25. Clarke, P. G., and R. W. Oppenheim. 1995. Neuron death in vertebrate development: in vivo methods. Methods Cell Biol. 46:277-321.
26. Clement, A. M., M. D. Nguyen, E. A. Roberts, M. L. Garcia, S. Boillée, M. Rule, et al. 2003. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-116.
27. Coleman, M. P., and V. H. Perry. 2002. Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci. 25:532-537.
28. Collard, J.-F., F. Côté, and J.-P. Jullen. 1995. Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375:61.
29. Conforti, L., R. Adalbert, and M. P. Coleman. 2007. Neuronal death: where does the end begin? Trends Neurosci. 30:159-166.
30. Cozzolino, M., A. Ferri, C. Valle, and M. T. Carrì. 2013. Mitochondria and ALS: implications from novel genes and pathways. Mol. Cell. Neurosci. 55:44-49.
31. Da Cruz, S., and D. W. Cleveland. 2011. Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr. Opin. Neurobiol. 21:904-919. doi: 10.1016/j.conb.2011.05.029. Epub 2 August 2011.
32. De Vos, K. J., A. L. Chapman, M. E. Tennant, C. Manser, E. L. Tudor, K. F. Lau, et al. 2007. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet. 16:2720-2728.
33. Del Gaizo, V., J. A. MacKenzie, and R. M. Payne. 2003. Targeting proteins to mitochondria using TAT. Mol. Genet. Metab. 80:170-180.
34. Dobrowolny, G., M. Aucello, M. Molinaro, and A. Musarò. 2008. Local expression of mIgf-1 modulates ubiquitin, caspase and CDK5 expression in skeletal muscle of an ALS mouse model. Neurol. Res. 30:131-136. doi: 10.1179/174313208X281235.
35. Drew, B., and C. Leeuwenburgh. 2003. Method for measuring ATP production is isolated mitochondria: ATP production in brain and liver mitochondria of Fischer-344 rats with age and caloric restriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285:R1259-R1267.
36. Ferri, A., J. R. Sanes, M. P. Coleman, J. M. Cunningham, and A. C. Kato. 2003. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr. Biol. 13:669-673.
37. Fischer, L. R., and J. D. Glass. 2007. Axonal degeneration in motor neuron disease. Neurodegener. Dis. 4:431-442. Epub 9 October 2007.
38. Fischer, L. R., D. G. Culver, P. Tennant, A. A. Davis, M. Wang, A. Castellano-Sanchez, et al. 2004. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 185:232-240.
39. Frey, D., C. Schneider, L. Xu, J. Borg, W. Spooren, and P. Caroni. 2000. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci. 20:2534-2542.
40. Friese, A., J. A. Kaltschmidt, D. R. Ladle, M. Sigrist, T. M. Jessell, and S. Arber. 2009. Gamma and alpha motor neurons distinguished by expression of transcription factor Err3. Proc. Natl. Acad. Sci. USA 106:13588-13593. doi: 10.1073/pnas.0906809106. Epub 2009 Jul 27.
41. Gerber, Y. N., J. C. Sabourin, M. Rabano, M. D. Vivanco, and F. E. Perrin. 2012. Early functional deficit and microglial disturbances in a mouse model of amyotrophic lateral sclerosis. PLoS One 7:e36000. doi: 10.1371/journal.pone.0036000. Epub 25 April 2012.
42. Gifondorwa, D. J., M. B. Robinson, C. D. Hayes, A. R. Taylor, D. M. Prevette, R. W. Oppenheim, et al. 2007. Exogenous delivery of heat shock protein 70 increases lifespan in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 27:13173-13180.
43. Gonatas, N. K., A. Stieber, and J. O. Gonatas. 2006. Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J. Neurol. Sci. 246:21-30.
44. Gould, T., and C. E. Milligan. 2012. Neuronal death & rescue: neurotrophic factors & anti-apoptotic mechanisms. Chapter 19 in M. Selzer, R. Miller, L. Cohen, S. Clarke and G. Kwakkel, eds. Textbook of neural repair & rehabilitation. Cambridge University Press, Cambridge. (In Press).
45. Gould, T. W., and R. W. Oppenheim. 2007. Synaptic dysfunction in disease and following injury in the developing and adult nervous system: caveats in the choice of therapeutic intervention. Neurosci. Biobehav. Rev. 31:1073-1087.
46. Gould, T. W., R. R. Buss, S. Vinsant, D. Prevette, W. Sun, C. M. Knudson, et al. 2006. Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J. Neurosci. 26:8774-8786.
47. Guégan, C., and S. Przedborski. 2003. Programmed cell death in amyotrophic lateral sclerosis. J. Clin. Invest. 111:153-161.
48. Gurney, M. E., H. Pu, A. Y. Chiu, M. C. Dal Canto, C. Y. Polchow, D. D. Alexander, et al. 1994. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772-1775.
49. Hafezparast, M., R. Klocke, C. Ruhrberg, A. Marquardt, A. Ahmad-Annuar, S. Bowen, et al. 2003. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808-810.
50. Hampton, T. G., and I. Amende. 2010. Treadmill gait analysis characterizes gait alterations in Parkinson's disease and amyotrophic lateral sclerosis mouse models. J. Mot. Behav. 42:1-4.
51. Hampton, T. G., M. R. Stasko, A. Kale, I. Amende, and A. C. Costa. 2004. Gait dynamics in trisomic mice: quantitative neurological traits of Down syndrome. Physiol. Behav. 82:381-389.
52. G93A mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 28:154-164.
53. Hellström, J., A. L. Oliveira, B. Meister, and S. Cullheim. 2003. Large cholinergic nerve terminals on subsets of motoneurons and their relation to muscarinic receptor type 2. J. Comp. Neurol. 460:476-486.
54. Kale, A., I. Amende, G. P. Meyer, J. C. Crabbe, and T. G. Hampton. 2004. Ethanol's effects on gait dynamics in mice investigated by ventral plane videography. Alcohol. Clin. Exp. Res. 28:1839-1848.
55. Karnovsky, M. J. 1964. The localization of cholinesterase activity in rat cardiac muscle by electron microscopy. J. Cell Biol. 23:217-232.
56. Kieran, D., M. Hafezparast, S. Bohnert, J. R. T. Dick, J. Martin, G. Schiavo, et al. 2005. A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J. Cell Biol. 169:561-567.
57. Kostic, V., V. Jackson-Lewis, F. de Bilbao, M. Dubois-Dauphin, and S. Przedborski. 1997. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 277:559-562.
58. LaMonte, B. H., K. E. Wallace, B. A. Holloway, S. S. Shelly, J. Ascano, M. Tokito, et al. 2002. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34:715-727.
59. Lee, Y., B. M. Morrison, Y. Li, S. Lengacher, M. H. Farah, P. N. Hoffman, et al. 2012. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443-448. doi: 10.1038/nature11314.
60. Libby, R. T., Y. Li, O. V. Savinova, J. Barter, R. S. Smith, R. W. Nickells, et al. 2005. Susceptibility to neurodegeneration in a glaucoma is modified by Bax gene dosage. PLoS Genet. 1:17-26.
61. Ligon, L. A., B. H. LaMonte, K. E. Wallace, N. Weber, R. G. Kalb, and E. L. Holzbaur. 2005. Mutant superoxide dismutase disrupts cytoplasmic dynein in motor neurons. Neuroreport 16:533-536.
62. Maeda, M., N. Ohba, S. Nakagomi, Y. Suzuki, S. Kiryu-Seo, K. Namikawa, et al. 2004. Vesicular acetylcholine transporter can be a morphological marker for the reinnervation to muscle of regenerating motor axons. Neurosci. Res. 48:305-314.
63. Mancuso, R., S. Oliván, R. Osta, and X. Navarro. 2011. Evolution of gait abnormalities in SOD1(G93A) transgenic mice. Brain Res. 1406:65-73.
64. Marinkovic, P., M. S. Reuter, M. S. Brill, L. Godinho, M. Kerschensteiner, and T. Misgeld. 2012. Axonal transport deficits and degeneration can evolve independently in mouse models of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 109:4296-4301. Epub 27 February 2012.
65. McKay, S. E., and R. W. Oppenheim. 1991. Lack of evidence for cell death among avian spinal cord interneurons during normal development and following removal of targets and afferents. J. Neurobiol. 22:721-733.
66. Mead, R. J., E. J. Bennett, A. J. Kennerley, P. Sharp, C. Sunyach, P. Kasher, et al. 2011. Optimised and rapid pre-clinical screening in the SOD1(G93A) transgenic mouse model of amyotrophic lateral sclerosis (ALS). PLoS One 6:e23244. doi: 10.1371/journal.pone.0023244. Epub 18 August 2011.
67. Medana, I. M., and M. M. Esiri. 2003. Axonal damage: a key predictor of outcome in human CNS diseases. Brain 126:515-530.
68. Miller, T. M., S. H. Kim, K. Yamanaka, M. Hester, P. Umapathi, H. Arnson, et al. 2006. Gene transfer demonstrates that muscle is not a primary target for non-cell-autonomous toxicity in familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 103:19546-19551. Epub 12 December 2006.
69. Mourelatos, Z., N. K. Gonatas, A. Stieber, M. E. Gurney, and M. C. Dal Canto. 1996. The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu, Zn superoxide dismutase becomes fragmented in early, preclinical stages. Proc. Natl. Acad. Sci. USA 93:5472-5477.
70. Oppenheim, R. W., C. Milligan, and C. von Bartheld. 2013. Programmed cell death and neurotrophic factors. Pp. 405-435 in L. R. Squire, ed. Fundamental neuroscience. 4th ed. Academic Press, San Diego.
71. Palop, J. J., J. Chin, and L. Mucke. 2006. A network dysfunction perspective on neurodegenerative diseases. Nature 443:768-773.
72. Pasinelli, P., and R. H. Brown. 2006. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nature 7:710-723.
73. Pedrini, S., D. Sau, S. Guareschi, M. Bogush, R. H. Jr Brown, N. Naniche, et al. 2010. ALS-linked mutant SOD1 damages mitochondria by promoting conformational changes in Bcl-2. Hum. Mol. Genet. 19:2974-2986.
74. Pestronk, A., and D. B. Drachman. 1978. Motor nerve sprouting and acetylcholine receptors. Science 199:1223-1225.
75. Peters, A., S. L. Palay, and H. Webster. 1991. Pp. 273-311 in Fine structure of the nervous system: neurons and their supporting cells. Oxford Univ. Press, NY.
76. Puls, I., C. Jonnakuty, B. LaMonte, E. Holbaur, M. Tokito, E. Mann, et al. 2003. Mutant dynactin in motor neuron disease. Nat. Genet. 33:455-456.
77. Pun, S., A. F. Santos, S. Saxena, L. Xu, and P. Caroni. 2006. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat. Neurosci. 9:408-419.
78. Rademakers, R., and M. van Blitterswijk. 2013. Motor neuron disease in 2012: novel causal genes and disease modifiers. Nat. Rev. Neurol. 9:63-64. doi: 10.1038/nrneurol.2012.276.
79. Raff, M. C., A. V. Whitmore, and J. T. Finn. 2002. Axonal self-destruction and neurodegeneration. Science 296:868-871.
80. Rizzoli, S. O., and W. J. Betz. 2004. The structural organization of the readily releasable pool of synaptic vesicles. Science 303:2037-2039.
81. Robinson, M. B., D. J. Gifondorwa, and C. Milligan. 2011. Mechanisms of the motoneuron stress response and its relevance in neurodegeneration. Pp. 45-62 in A. S. McNeill, ed. Neurodegeneration: theory, disorders and treatments. NovaPublishers, Hauppauge, NY.
82. Rothstein, J. D. 2009. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann. Neurol. 65(Suppl. 1):S3-S9.
83. Sagot, Y., M. Dubois-Dauphin, S. A. Tan, F. de Bibao, P. Aebischer, J.-C. Martinou, et al. 1995. Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of neurodegenerative disease. J. Neurosci. 15:7727-7733.
84. Sánchez-Carbente, M. R., S. Castro-Obregón, L. Covarrubias, and V. Narváez. 2005. Motoneuronal death during spinal cord development is mediated by oxidative stress. Cell Death Differ. 12:279-291.
85. Sasaki, S., H. Warita, K. Abe, and M. Iwata. 2004. Slow component of axonal transport is impaired in the proximal axon of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol. 107:452-460.
86. Sathasivam, S., and P. J. Shaw. 2005. Apoptosis in amyotrophic lateral sclerosis - what is the evidence? Lancet Neurol. 4:500-509.
87. Saxena, S., and P. Caroni. 2007. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 83:174-191.
88. Saxena, S., and P. Caroni. 2011. Selective neuronal vulnerability in neurodegenerative diseases: from stressor thresholds to degeneration. Neuron 71:35-48. doi: 10.1016/j.neuron.2011.06.031.
89. Saxena, S., E. Cabuy, and P. Caroni. 2009. A role for motoneuron subtype-selective ER stress in disease manifestations of fALS mice. Nat. Neurosci. 12:627-636.
90. Schikorski, T., and C. F. Stevens. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17:5858-5867.
91. Schikorski, T., and C. F. Stevens. 2001. Morphological correlates of functionally defined synaptic vesicle populations. Nat. Neurosci. 4:391-395.
92. Schon, E. A., and S. Przedborski. 2011. Mitochondria: the next (neurode)generation. Neuron 70:1033-1053.
93. Scott, S., J. E. Kranz, J. Cole, J. M. Lincecum, K. Thompson, N. Kelly, et al. 2008. Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph. Lateral Scler. 9:4-15.
94. Shneider, N. A., M. N. Brown, C. A. Smith, J. Pickel, and F. J. Alvarez. 2009. Gamma motor neurons express distinct genetic markers at birth and require muscle spindle-derived GDNF for postnatal survival. Neural Dev. 4:42. doi:10.1186/1749-8104-4-42
95. Siklós, L., J. Engelhardt, Y. Harati, R. G. Smith, F. Joó, and S. H. Appel. 1996. Ultrastructural evidence for altered calcium in motor nerve terminals in amyotrophic lateral sclerosis. Ann. Neurol. 39:203-216.
96. Stieber, A., Y. Chen, S. Wei, Z. Mourelatos, J. Gonatas, K. Okamoto, et al. 1998. The fragmented neuronal Golgi apparatus in amyotrophic lateral sclerosis includes the trans-Golgi-network: functional implications. Acta Neuropathol. 95:245-253.
97. Suzuki, M., J. McHaugh, C. Tork, B. Shelley, S. M. Klein, P. Aebischer, et al. 2007. GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS. PLoS One 8:1-14.
98. Tömböl, T., G. Pataki, A. Németh, and J. Hamar. 2002. Ultrastructural changes of the neuromuscular junction in reperfusion injury. Cells Tissues Organs 170:139-150.
99. Truett, G. E., P. Heeger, R. L. Mynatt, A. A. Truett, J. A. Walker, and M. L. Warman. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29:52, 54.
100. Tsujihata, M., R. Hazama, T. Yoshimura, A. Satoh, M. Mori, and S. Nagataki. 1984. The motor end-plate fine structure and ultrastructural localization of acetylcholine receptors in amyotrophic lateral sclerosis. Muscle Nerve 7:243-249.
101. Turner, B. J., and K. Talbot. 2008. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog. Neurobiol. 85:94-134.
102. Tyler, W. J., and L. D. Pozzo-Miller. 2001. BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J. Neurosci. 21:4249-4258.
103. Uchizono, K. 1965. Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 207:642-643.
104. Uchizono, K. 1966. Excitatory and inhibitory synapses in the cat spinal cord. Jpn. J. Physiol. 16:570-575.
105. Valdez, G., J. C. Tapia, J. W. Lichtman, M. A. Fox, and J. R. Sanes. 2012. Shared resistance to aging and ALS in neuromuscular junctions of specific muscles. PLoS One 7:e34640. doi: 10.1371/journal.pone.0034640. Epub 2 April 2012.
106. Vargas, M. R., and J. A. Johnson. 2010. Astrogliosis in amyotrophic lateral sclerosis: role and therapeutic potential of astrocytes. Neurotherapeutics 7:471-481. doi: 10.1016/j.nurt.2010.05.012.
107. Warita, H., Y. Itoyama, and K. Abe. 1999. Selective impairment of fast anterograde axonal transport in the peripheral nerves of asymptomatic transgenic mice with a G93A mutant SOD1 gene. Brain Res. 819:120-131.
108. Whitehead, N. P., M. Streamer, L. I. Lusambili, F. Sachs, and D. G. Allen. 2006. Streptomycin reduces stretch-induced membrane permeability in muscles from mdx mice. Neuromuscul. Disord. 16:845-854.
109. Williamson, T. L., and D. W. Cleveland. 1999. 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.
110. Yamanaka, K., S. Boillee, E. A. Roberts, M. L. Garcia, M. McAlonis-Downes, O. R. Mikse, et al. 2008a. Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. PNAS 105:7594-7599.
111. Yamanaka, K., S. J. Chun, S. Boillee, N. Fujimori-Tonou, H. Yamashita, D. H. Gutmann, et al. 2008b. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci. 11:251-253.
112. Zhang, B., P.-H. Tu, F. Abtahian, J. Q. Trojanowski, and V. M.-Y. Lee. 1997. 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.
113. Zhu, T., L. Zhou, S. Mori, Z. Wang, C. F. McTiernan, C. Qiao, et al. 2005. Sustained whole-body functional rescue in congestive heart failure and muscular dystrophy hamsters by systemic gene transfer. Circulation 112:2650-2659.