Oxidative stress, mutant SOD1, and neurofilament patholooy in transgenic mouse models of human motor neuron disease

Laboratory Investigation

Volumn 76, Issue 4, 1997, Pages 441-456

  Tu, Pang Hsien ^a   Gurney, Mark E ^b   Julien, Jean Pierre ^c   Lee, Virginia M Y ^a   Trojanowski, John Q ^a,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b PFIZER INC   (United States)

^c MONTREAL GENERAL HOSPITAL   (Canada)

^d HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; COPPER ZINC SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ENDOPLASMIC RETICULUM; MOTOR NEURON DISEASE; MOUSE; NEUROFILAMENT; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; HUMANS; MICE; MICE, TRANSGENIC; NEUROFIBRILS; OXIDATIVE STRESS; POINT MUTATION; SUPEROXIDE DISMUTASE;

EID: 0030910404     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (123)

1. Abe K, Pan LH, Watanabe M, Kato T, and Itoyama Y (1995). Induction of nitrotyrosine-like immunoreactivity in the lower motor neuron of amyotrophic lateral sclerosis. Neurosci Lett 199:152-154.
2. Andersen PM, Nilsson P, Ala-Hurula V, Keranen ML, Tarvainen I, Haltia T, Nilsson L, Binzer M, Forsgren L, and Marklund SL (1995). Amyotrophic lateral sclerosis associated with homozygosity for an Asp90Ala Mutation in Cu/Zn superoxide dismutase. Nat Genet 10:61-66.
3. Aoki M, Ogasawara M, Matsubara Y, Narisawa K, Nakamura S, Itoyama Y, and Abe K (1994). Familial amyotrophic lateral sclerosis (ALS) in Japan associated with H46R mutation in Cu/Zn superoxide dismutase gene: A possible new subtype of familial ALS. J Neurol Sci 126:77-83.
4. Avraham KB, Schickler M, Sapoznikov D, Yarom R, and Groner Y (1988). Down's syndrome: Abnormal neuromuscular junction in tongue of transgenic mice with elevated levels of human Cu/Zn-superoxide dismutase. Cell 54:823-829.
5. Avraham KB, Sugarman H, Rotshenker S, and Groner Y (1991). Down's syndrome: Morphological remodelling and increased complexity in the neuromuscular junction of transgenic Cu/Zn-superoxide dismutase mice. J Neurocytol 20: 208-215.
6. Balin BJ and Lee VM (1991). Individual neurofilament subunits reassembled in vitro exhibit unique biochemical, morphological and immunological properties. Brain Res 556: 196-208.
7. Barkats M, Bertholet JY, Venault P, Ceballos-Picot I, Nicole A, Phillips J, Moutier R, Roubertoux P, Sinet PM, and Cohen-Salmon C (1993). Hippocampal mossy fiber changes in mice transgenic for the human copper-zinc superoxide dismutase gene. Neurosci Lett 160:24-28.
8. Beckman JS, Carson M, Smith CD, and Koppenol WH (1993). ALS, SOD and peroxynitrite (letter). Nature 364:584.
9. Beckman JS, Chen J, Crow JP, and Ye YZ (1994). Reactions of nitric oxide, superoxide and peroxynitrite with superoxide dismutase in neurodegeneration. Prog Brain Res 103:371-380.
10. Bergeron C, Petrunka C, and Weyer L (1996). Copper/zinc superoxide dismutase expression in the human central nervous system: Correlation with selective neuronal vulnerability. Am J Pathol 148:273-279.
11. Boisvert DPJ and Schreiber C (1992). Interrelationship of excitotoxic and free radical mechanisms. In: Krieglstein J and Oberpichler H, editors: Pharmacology of cerebral ischemia. Stuttgart, Germany: Wissenshaftliche Verlagsgesellschaft mbH, 1-10.
12. Borchelt DR, Lee MK, Slunt HS, Guarnieri M, Xu ZS, Wong PC, Brown RH Jr, Price DL, Sisodia SS, and Cleveland DW (1994). Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci USA 91:8292-8296.
13. Bowling AC, Schulz JB, Brown RH Jr, and Beal MF (1993). Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis. J Neurochem 61:2322-2325.
14. Brown RH Jr (1995). Amyotrophic lateral sclerosis: Recent insights from genetics and transgenic mice. Cell 80:687-692.
15. Bull PC, Thomas GR, Rommens JM, Forbes JR, and Cox DW (1993). The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet 5:327-337.
16. Cadet JL, Ladenheim B, Baum I, Carlson E, and Epstein C (1994a). Cu/Zn-superoxide dismutase (Cu/ZnSOD) transgenic mice show resistance to the lethal effects of methylenedioxyamphetamine (MDA) and of methylenedioxymethamphetamine (MDMA). Brain Res 655:259-262.
17. Cadet JL, Sheng P, Alis S, Rothman R, Carlson E, and Epstein C (1994b). Attenuation of methamphetamine-induced neurotoxicity in copper/zinc superoxide dismutase transgenic mice. J Neurochem 62:380-383.
18. Callahan CA and Thomas JB (1994). Tau-β-galactosidase, an axon-targeted fusion protein. Proc Natl Acad Sci USA 91: 5972-5976.
19. Carden MJ and Eagles PAM (1986). Chemical cross-linking analyses of ox neurofilaments. Biochem J 234:587-591.
20. Cheng L, Watt R, and Piper PW (1994). Polyubiquitin gene expression contributes to oxidative stress resistance in respiratory yeast (Saccharomyces cerevisiae). Mol Gen Genet 243:358-362.
21. Ching GY and Liem RKH (1993). Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments. J Cell Biol 122:1323-1335.
22. Chio A, Brignolio F, Meinen P, and Schiffer D (1987). Phenotypic and genotypic heterogeneity of dominantly inherited amyotrophic lateral sclerosis. Acta Neurol Scand 75:277-282.
23. Chou SM, Wang HS, and Komai K (1996). Colocalization of NOS and SOD1 in neurofilament accumulation with motor neurons of amyotrophic lateral sclerosis: An immunohistochemical study. J Chem Neuroanat 10:249-258.
24. Christiano F, de Haan JB, Iannello RC, and Kola I (1995). Changes in the levels of enzymes which modulate the antioxidant balance occur during aging and correlate with cellular damage. Mech Ageing Dev 80:93-105.
25. Collard JF, Côté F, and Julien JP (1995). Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375:61-64.
26. Côté F, Collard JF, and Julien JP (1993). Progressive neuronopathy in transgenic mice expressing the human neurofilament heavy gene: A mouse model of amyotrophic lateral sclerosis. Cell 73:35-46.
27. Culotta VC, Joh HD, Lin SJ, and Slekar KH (1995). A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. J Biol Chem 270:29991-29997.
28. Dal Canto MC and Gurney ME (1994). Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am J Pathol 145:1271-1280.
29. Dal Canto MC and Gurney ME (1995). 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 676:25-40.
30. Danks DM (1989). Disorders of copper transport. In: Scriver CR, Beaudet AL, Sly WS, and Valle D, editors. The metabolic basis of inherited disease. New York: McGraw-Hill, 1411-1431.
31. Davies KJ and Delsignore ME (1987). Protein damage and degradation by oxygen radicals: III - Modification of secondary and tertiary structure. J Biol Chem 262:9908-9913.
32. de Belleroche J, Orrell RW, and Virgo L (1996). Amyotrophic lateral sclerosis: Recent advances in understanding disease mechanisms. J Neuropathol Exp Neurol 55:747-757.
33. de Haan JB, Cristiano F, Iannello RC, and Kola I (1995). Cu/Zn-superoxide dismutase and glutathione peroxidase during aging. Biochem Mol Biol Int 35:1281-1297.
34. de Haan JB, Newman JD, and Kola I (1992). Cu/Zn superoxide dismutase mRNA and enzyme activity, and susceptibility to lipid peroxidation, increases with aging in murine brains. Mol Brain Res 13:179-187.
35. Deng HX, Hentati A, Tainer JA, Iqbal Z, Cayabyab A, Hung WY, Getzoff ED, Hu P, Herfeldt B, Roos RP, Warner C, Deng G, Soriano E, Smyth C, Parge HE, Ahmed A, Roses AD, Hallewell RA, Pericak-Vance MA, and Siddique T (1993). Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science 261:1047-1051.
36. Eisen A (1995). Amyotrophic lateral sclerosis is a multifactorial disease. Muscle Nerve 18:741-752.
37. Eisen A and Krieger C (1993). Pathogenic mechanisms in sporadic amyotrophic lateral sclerosis. Can J Neurol Sci 20:286-296.
38. Elroy-Stein O and Groner Y (1988). Impaired neurotransmitter uptake in PC12 cells overexpressing human Cu/Zn-superoxide dismutase-implications for gene dosage effects in Down's syndrome. Cell 52:259-267.
39. Emery AEH and Holloway S (1982). Familial motor neuron disease. In: Rowland LP, editor. Human motor neuron diseases. New York: Raven Press, 139-147.
40. Enayat ZE, Orrell RW, Claus A, Ludolph A, Bachus R, Brockmuller J, Ray-Chaudhuri K, Radunovic A, Shaw C, Wilkinson J, King A, Swash M, Leigh PN, de Belleroche J, and Powell J (1995). Two novel mutations in the gene for copper zinc superoxide dismutase in UK families with amyotrophic lateral sclerosis. Hum Mol Genet 4:1239-1240.
41. Esteban J, Rosen DR, Bowling AC, Sapp P, McKenna-Yasek D, O'Regan JP, Beal MF, Horvitz HR, and Brown RH Jr (1994). Identification of two novel mutations and a new polymorphism in the gene for Cu/Zn superoxide dismutase in patients with amyotrophic lateral sclerosis. Hum Mol Genet 3:997-998.
42. Eyer J and Peterson A (1994). Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a neurofilament-β-galactosidase fusion protein. Neuron 12:389-405.
43. Fielden EM, Roberts PB, Bray RC, Lowe DJ, Mautner GN, Rotilio G, and Calabrese L (1974). The mechanism of action of superoxide dismutase from pulse radiolysis and electron paramagnetic resonance. Biochem J 139:49-60.
44. Figlewicz DA, Krizus A, Martinoli MG, Meininger V, Dib M, Rouleau GA, and Julien JP (1994). Variants of the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis. Hum Mol Genet 3:1757-1761.
45. Figueiredo-Pereira ME, Berg KA, and Wilk S (1994). A new inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces accumulation of ubiquitin-protein conjugates in a neuronal cell. J Neurochem 63:1578-1581.
46. Gaczynska M, Rock KL, and Goldberg AL (1993). g-interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature 365:264-267.
47. Geisler N, Kaufmann E, Fischer S, Plessman U, and Weber K (1983). Neurofilament architecture combines structural principles of intermediate filaments with carboxyl-terminal extensions increasing in size between triplet proteins. EMBO J 2:1295-1302.
48. Getzoff ED, Trainer JA, Stempien MM, Bell GI, and Hallewell RA (1989). Evolution of Cu/Zn superoxide dismutase and the Greek β-barrel structure motif. Prot Struct Funct Genet 5:322-336.
49. Giulivi C and Davies KJA (1994). Dityrosine: A marker for oxidatively modified proteins and selective proteolysis. Methods Enzymol 233:363-371.
50. Jones CT, Shaw PJ, Chari G, and Brock DJ (1994b). Identification of a novel exon 4 SOD1 mutation in a sporadic amyotrophic lateral sclerosis patient. Mol Cell Probes 8:329-330.
51. Jones CT, Swingler RJ, and Brock DJ (1994a). Identification of a novel SOD1 mutation in an apparently sporadic amyotrophic lateral sclerosis patient and the detection of lle113Thr in three others. Hum Mol Genet 3:649-650.
52. Jungmann J, Reins HA, Schobert C, and Jentsch S (1993). Resistance to cadmium mediated by ubiquitin-dependent proteolysis. Nature 361:369-371.
53. Kato S, Shimoda M, Watanabe Y, Nakashima K, Takahashi K, and Ohama E (1996). Familial amyotrophic lateral sclerosis with a two base pair deletion in superoxide dismutase 1 gene: Multisystem degeneration with intracytoplasmic hyaline inclusions in astrocytes. J Neuropathol Exp Neurol 55: 1089-1101.
54. Kobashi K (1968). Catalytic oxidation of sulfhydryl groups by o-phenanthroline copper complex. Biochem Biophys Acta 158:239-245.
55. Kominami K, DeMartino GN, Moomaw CR, Slaughter CA, Shimbara N, Fujimuro M, Yokosawa H, Hisamatsu H, Tanahashi N, Shimizu Y, Tanaka K, and Toh-e A (1995). Nin1p, a regulatory subunit of the 26S proteasome is necessary for activation of Cdc28p kinase of Saccharomyces cerevisiae. EMBO J 14:3105-3115.
56. 2 peptide. Proc Natl Acad Sci USA 93:3377-3382.
57. Lee MK, Marszalek JR, and Cleveland DW (1994). A mutant neurofilament subunit causes massive selective motor neuron death: Implications for the pathogenesis of human motor neuron disease. Neuron 13:975-988.
58. Lee MK, Xu Z, Wong PC, and Cleveland DW (1993). Neurofilaments are obligate heteropolymers in vivo. J Cell Biol 122:1337-1350.
59. Leterrier JF, Langui D, Probst A, and Ulrich J (1992). A molecular mechanism for the induction of neurofilament bundling by aluminum ions. J Neurochem 58:2060-2070.
60. Li TM, Alberman E, and Swash M (1988). Comparison of sporadic and familial disease amongst 580 cases of motor neuron disease. J Neurol Neurosurg Psychiatry 51:778-784.
61. Lowe J, Mayer RJ, and Landon M (1993). Ubiquitin in neurodegenerative diseases. Brain Pathol 3:55-65.
62. McCay PB (1985). Vitamin E: Interactions with free radicals and ascorbate. Ann Rev Nutr 5:323-340.
63. Michalek MT, Grant EP, Gramm C, Goldberg AL, and Rock KL (1993). A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature 363:552-554.
64. Mitchell JD, Gatt JA, Phillips TM, Houghton E, Rostron G, Whittington J, and Shaw IC (1993). Cu/Zn superoxide dismutase free radicals, and motoneuron disease. Lancet 342: 1051-1052.
65. Montine TJ, Farris DB, and Graham DG (1995). Covalent crosslinking of neurofilament proteins by oxidized catechols as a potential mechanism of Lewy body formation. J Neuropathol Exp Neurol 54:311-319.
66. Morrison BM, Gordon JW, Ripps ME, and Morrison JH (1996). Quantitative immunocytochemical analysis of the spinal cord in G86R superoxide dismutase transgenic mice: Neurochemical correlates of selective vulnerability. J Comp Neurol 373:619-631.
67. Mourelatos Z, Gonatas NK, Stieber A, Gurney ME, and Dal Canto MC (1996). The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu, Zn superoxide dismutase becomes fragmented in early, preclinical stages of the disease. Proc Natl Acad Sci USA 93:5472-5477.
68. Mu X, He J, Anderson DW, Trojanowski JQ, and Springer JE (1996). Altered expression of bcl-2 and bax mRNA in amyotrophic lateral sclerosis spinal cord motor neurons. Ann Neurol 40:379-386.
69. Nabarra B, Casanova M, Paris D, Nicole A, Toyama K, Sinet P-M, Ceballos I, and London J (1996). Transgenic mice overexpressing the human Cu/Zn-SOD gene: Ultrastructural studies of a premature thymic involution model of Down's syndrome (Trisomy 21). Lab Invest 74:617-626.
70. Nakashima K, Watanabe Y, Kuno N, Nanba E, and Takahashi K (1995). Abnormality of Cu/Zn superoxide dismutase (SOD1) activity in Japanese familial amyotrophic lateral sclerosis with two base pair deletion in the SOD1 gene. Neurology 45: 1019-1020.
71. Nixon RA (1993). The regulation of neurofilament protein dynamics by phosphorylation: Clues to neurofibrillary pathobiology. Brain Pathol 3:29-38.
72. Olanow CW and Arendash GW (1994). Metals and free radicals in neurodegeneration. Curr Opin Neurol 7:548-558.
73. Orr WC and Sohal RS (1994). Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263:1128-1130.
74. Orrell R, de Belleroche J, Marklund S, Bowe F, and Hallewell R (1995a). A novel SOD mutant and ALS. Nature 374:504-505.
75. Orrell RW, King AW, Hilton DA, Campbell MJ, Lane RJM, and de Belleroche JS (1995b). Familial amyotrophic lateral sclerosis with a point mutation of SOD-1: Intrafamilial heterogeneity of disease duration associated with neurofibrillary tangles. J Neurol Neurosurg Psychiatry 59:266-270.
76. Oury TD, Tatro L, Ghio AJ, and Piantadosi CA (1995). Nitration of tyrosine by hydrogen peroxide and nitrite. Free Radical Res 23:537-547.
77. Pardo CA, Xu Z, Borchelt DR, Price DL, Sisodia SS, and Cleveland DW (1995). Superoxide dismutase is an abundant component in cell bodies, dendrites, and axons of motor neurons and in a subset of other neurons. Proc Natl Acad Sci USA 92:954-958.
78. Peled-Kamar M, Lotem J, Okon E, Sachs L, and Groner Y (1995). Thymic abnormalities and enhanced apoptosis of thymocytes and bone marrow cells in transgenic mice overexpressing Cu/Zn-superoxide dismutase: Implications for Down's syndrome. EMBO J 14:4985-4993.
79. Pelligrini-Giampietro DE, Cherici G, Alesiani M, Carla V, and Moroni F (1990). Excitatory amino acid release and free radical formation may cooperate in the genesis of ischemia-induced neuronal damage. J Neurosci 10:1035-1041.
80. Phillips JP, Tainer JA, Getzoff ED, Boulianne GL, Kirby K, and Hilliker AJ (1995). Subunit-destabilizing mutations in Drosophila copper/zinc superoxide dismutase: Neuropathology and a model of dimer dysequilibrium. Proc Natl Acad Sci USA 92:8574-8578.
81. Pollanen MS, Dickson DW, and Bergeron C (1993). Pathology and biology of the Lewy body. J Neuropathol Exp Neurol 52:183-191.
82. Pramatarova A, Figlewicz DA, Krizus A, Han FY, Ceballos-Picot I, Nicole A, Dib M, Meininger V, Brown RH, and Rouleau GA (1995). Identification of new mutations in the Cu/Zn superoxide dismutase gene of patients with familial amyotrophic lateral sclerosis. Am J Hum Genet 56:592-596.
83. Pramatarova A, Goto J, Eiji N, Nakashima K, Takahashi K, Takagi A, Kanazawa I, Figlewicz DA, and Rouleau GA (1994). A two basepair deletion in the SOD1 gene causes familial amyotrophic lateral sclerosis. Hum Mol Genet 3:2061-2062.
84. Przedborski S, Donaldson D, Jakowec M, Kish SJ, Guttman M, Rosoklija G, and Hays AP (1996). Brain superoxide dismutase, catalase, and glutathione peroxidase activities in amyotrophic lateral sclerosis. Ann Neurol 39:158-165.
85. Rabizadeh S, Gralla EB, Borchelt DR, Gwinn R, Valentine JS, Sisodia S, Wong P, Lee M, Hahn H, and Bredesen DE (1995). Mutations associated with amyotrophic lateral sclerosis convert superoxide dismutase from an antiapoptotic gene to a proapoptotic gene: Studies in yeast and neural cells. Proc Natl Acad Sci USA 92:3024-3028.
86. Ripps ME, Huntley GW, Hof PR, Morrison JH, and Gordon JW (1995). Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 92: 689-693.
87. Rivett AJ (1985). Purification of a liver alkaline protease which degrades oxidatively modified glutamine synthetase: Characterization as a high molecular weight cysteine proteinase. J Biol Chem 260:12600-12606.
88. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D, and Goldberg AL (1994). Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78:761-771.
89. Rosen DR, Siddique T, Patterson D, Figlewicz D A, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston SM, Berger R, Tanzi RE, Halperin JJ, Herzfeldt B, Van den Bergh R, Hung WY, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vance MA, Haines J, Rouleau GA, Gusella JS, Horvitz HR, and Brown RH Jr (1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362: 59-62.
90. Rothstein JD, Bristol LA, Hosler B, Brown RH Jr, and Kuncl RW (1994). Chronic inhibition of superoxide dismutase produces apoptotic death of spinal neurons. Proc Natl Acad Sci USA 91:4155-4159.
91. Rouleau GA, Clark AW, Rooke K, Pramatarova A, Krizus A, Suchowersky O, Julien JP, and Figlewicz D (1996). SOD1 mutation is associated with accumulation of neurofilaments in amyotrophic lateral sclerosis. Ann Neurol 39:128-131.
92. Schmidt ML, Carden MJ, Lee VMY, and Trojanowski JQ (1987). Phosphate-dependent and -independent neurofilament epitopes in the axonal swellings of patients with motor neuron disease and controls. Lab Invest 56:282-294.
93. Schmidt ML, Murray J, Lee VMY, Hill WD, and Trojanowski JQ (1991). Epitope map of neurofilament protein domains in cortical and peripheral nervous system Lewy bodies. Am J Pathol 139:53-65.
94. Scott MD, Meshnick SR, and Eaton JW (1987). Superoxide dismutase-rich bacteria: Paradoxical increase in oxidant toxicity. J Biol Chem 262:3640-3645.
95. Seto NO, Hayashi S, and Tener GM (1990). Overexpression of Cu-Zn superoxide dismutase in drosophila does not affect life-span. Proc Natl Acad Sci USA 87:4270-4274.
96. Sette M, Paci M, Desideri A, and Rotilio G (1995). A two-dimensional NMR study of bovine Cu, Co superoxide dismutase further assignments in the region surrounding the active site. Eur J Biochem 227:441-447.
97. Shang F and Taylor A (1995). Oxidative stress and recovery from oxidative stress are associated with altered ubiquitin conjugating and proteolytic activities in bovine lens epithelial cells. Biochem J 307:297-303.
98. Siddique T (1991). Molecular genetics of familial amyotrophic lateral sclerosis. In: Rowland LP, editor: Amyotrophic lateral sclerosis and other motor neuron disease. Adv Neurol 56: 227-231.
99. Själander A, Beckman G, Deng HX, Iqbal Z, Tainer JA, and Siddique T (1995). The D90A mutation results in a polymorphism of Cu, Zn superoxide dismutase that is prevalent in northern Sweden and Finland. Hum Mol Genet 4:1105-1108.
100. Sohal RS, Agarwal A, Agarwal S, and Orr WC (1995). Simultaneous overexpression of copper and zinc-containing superoxide dismutase and catalase retards age-related oxidative damage and increases metabolic potential in Drosophila melanogaster. J Biol Chem 270:15671-15674.
101. Spencer PS, and Griffin JW (1982). Disruption of axoplasmic transport by neurotoxic agents: The 2:5-hexanedione model. In: Weiss DG and Gorio A, editors. Axoplasmic transport in physiology and pathology. Berlin: Springer-Verlag, 92-103.
102. St Clair MBG, Anthony DC, Wikstrand CJ, and Graham DG (1989). Neurofilament protein crosslinking in γ-diketone neuropathy: In vitro and in vivo studies using the seaworm Myxicola infundibulum. Neurotoxicology 10:743-756.
103. Sternlieb I, Quintana N, Volenberg I, and Schilsky ML (1995). An array of mitochondrial alterations in the hepatocytes of Long-Evans Cinnamon rats. Hepatology 22:1782-1787.
104. Tainer JA, Getzoff ED, Beem KM, Richardson JS, and Richardson DC (1982). Determination and analysis of the 2A structure of copper and zinc superoxide dismutase. J Mol Biol 160:181-217.
105. Takahashi H, Makifuchi T, Nakano R, Sato S, Inuzaka T, Sakinura K, Mishua M, Honna Y, Osuji S, and Ikuta F (1994). Familial amyotrophic lateral sclerosis with a mutation in the Cu/Zn superoxide dismutase gene. Acta Neuropathol (Berl) 88:185-188.
106. Treier M, Staszewski LM, and Bohmann (1994). Ubiquitin-dependent c-Jun degradation in vivo is mediated by the 8 domain. Cell 78:787-798.
107. Trojanowski JQ and Lee VMY (1994). Phosphorylation of neuronal cytoskeletal proteins in Alzheimer's disease and Lewy body dementias. Ann N Y Acad Sci 747:92-109.
108. Troy CM, Derossi D, Prochiantz A, Greene LA, and Shelanski ML (1996). Downregulation of Cu/Zn superoxide dismutase leads to cell death via the nitric oxide-peroxynitrite pathway. J Neurosci 16:253-261.
109. Troy CM and Shelanski ML (1994). Down-regulation of copper/zinc superoxide dismutase causes apoptotic death in PC12 neuronal cells. Proc Natl Acad Sci USA 91:6384-6387.
110. Tsuda T, Munthasser S, Fraser PE, Percy ME, Rainero I, Vaula G, Pinessi L, Bergamini L, Vignocchi G, Crapper McLachlan DR, Tatton WG, and St George-Hyslop P (1994). Analysis of the functional effects of a mutation in SOD1 associated with familial amyotrophic lateral sclerosis. Neuron 13:727-736.
111. Tu PH and Lee VMY (1997, in press). Neurofilaments: Structure, function and involvement in neurodegeneration. Adv Mol Cell Biol.
112. Tu PH, Raju P, Robinson KA, Gurney ME, Trojanowski JQ, and Lee VMY (1996). Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc Natl Acad Sci USA 93:3155-3160.
113. Tu PH, Robinson KA, de Snoo F, Eyer J, Peterson AC, Lee VMY, and Trojanowski JQ (1997). Selective degeneration of Purkinje cells with Lewy body-like inclusions in aged NF-HLacZ transgenic mice. J Neurosci 17:1064-1074.
114. van der Vliet A, Eiserich JP, O'Neill CA, Halliwell B, and Cross CE (1995). Tyrosine modification by reactive nitrogen species: A closer look. Arch Biochem Biophys 319:341-349.
115. Ward CL, Omura S, and Kopito RR (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83:121-127.
116. Wenzel T, and Baumeister W (1993). Thermoplasma acidophilum proteasomes degrade partially unfolded and ubiquitin-associated proteins. FEBS Lett 326:215-218.
117. White CW, Avraham KB, Shanley PF, and Groner Y (1991). Transgenic mice with expression of elevated levels of copper-zinc superoxide dismutase in the lungs are resistant to pulmonary oxygen toxicity. J Clin Invest 87:2162-2168.
118. Wiedau-Pazos M, Goto JJ, Rabizadeh S, Gralla EB, Roe JA, Lee MK, Valentine JS, and Bredesen DE (1996). Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science 271:515-518.
119. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, Sisodia SS, Cleveland DW, and 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.
120. Wu J, Forbes JR, Chen HS, and Cox DW (1994). The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene. Nat Genet 7:541-545.
121. Xu Z, Cork LC, Griffin JW, and Cleveland DW (1993). Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell 73:23-33.
122. m for hydrogen peroxide. Proc Natl Acad Sci USA 93:5709-5714.
123. Yulug IG, Katsanis N, de Belleroche J, Collinge J, and Fischer EMC (1995). An improved protocol for the analysis of SOD1 gene mutations, and a new mutation in exon 4. Hum Mol Genet 4:1101-1104.