Role of zinc in ALS

Amyotrophic Lateral Sclerosis

Volumn 8, Issue 3, 2007, Pages 131-143

  Smith, Andrew P ^a   Lee, Nancy M ^a  

^a CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

Author keywords

ALS; Glutamate excitotoxicity; Metallothionein; Neuroinflammation; Oxidative stress; Protein aggregation; Zinc; Zinc transporter

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GLUTAMIC ACID; GROWTH FACTOR; METALLOTHIONEIN; ZINC ION; ZINC TRANSPORTER;

AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; AUTOPSY; DEGENERATIVE DISEASE; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENCEPHALITIS; ENVIRONMENTAL FACTOR; EXCITOTOXICITY; GENE EXPRESSION; GENE MUTATION; GUAM; HUMAN; MICROGLIA; NEUROFILAMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; REVIEW; WAR;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; GLUTAMIC ACID; HUMANS; MITOCHONDRIA; OXIDATIVE STRESS; ZINC;

EID: 34250000562     PISSN: 17482968     EISSN: 1471180X     Source Type: Journal    
DOI: 10.1080/17482960701249241     Document Type: Review

References (188)

1. Ferrante, R. J., Browne, S. E., Shinobu, L. A., Bowling, A. C., Baik, M. J. and MacGarvey, U. (1997) Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J Neurochem, 69, pp. 2064-2074.
2. Liu, R., Althaus, J. S., Ellerbock, B. R., Becker, D. A. and Gurney, M. E. (1998) Enhanced oxygen radical production in a transgenic mouse model of familial amyotrophic lateral sclerosis. Ann Neurol, 44, pp. 763-770.
3. Pedersen, W. A., Fu, W., Keller, J. N., Markesbery, W. R., Appel, S. and Smith, R. G. (1998) Protein modification by the lipid peroxidation product 4-hydroxynonenal in the spinal cords of amyotrophic lateral sclerosis patients. Ann Neurol, 44, pp. 819-824.
4. Shibata, N. (2001) Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Neuropathol, 21, pp. 82-92.
5. Chung, Y. H., Joo, K. M., Lee, Y. J., Kim, M. J. and Cha, C. I. (2003) Immunohistochemical study on the aggregation of ubiquitin in the central nervous system of transgenic mice expressing a human Cu/Zn SOD mutation. Neurol Res, 25, pp. 395-400.
6. Almer, G., Vukosavic, S., Romero, N. and Przedborski, S. (1999) Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem, 72, pp. 2415-2425.
7. Jokic, N., Scala, F. Di, Dupuis, L., Rene, F., Muller, A. and De Aguilar, J. L. (2003) Early activation of antioxidant mechanisms in muscle of mutant Cu/Zn-superoxide dismutase-linked amyotrophic lateral sclerosis mice. Ann N.Y. Acad Sci, 1010, pp. 552-558.
8. Chen, L. -C., Smith, A. P., Ben, Y., Zukic, B., Ignacio, S. and Moore, D. (2004) Temporal gene expression patterns in G93A/SOD1 mouse. Amyotroph Lateral Scler Other Motor Neuron Disord, 11, pp. 1-8.
9. Kiaei, M., Kipiani, K., Petri, S., Choi, D. K., Chen, J. and Calingasan, N. Y. (2005) Integrative role of cPLA with COX-2 and the effect of non-steroidal anti-inflammatory drugs in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurochem, 93, pp. 403-411.
10. Klivenyi, P., Kiaei, M., Gardian, G., Calingasan, N. Y. and Beal, M. F. (2004) Additive neuroprotective effects of creatine and cyclooxygenase 2 inhibitors in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurochem, 88, pp. 576-582.
11. Shaw, P. J. and Williams, R. (2000) Serum and cerebrospinal fluid biochemical markers of ALS. Amyotroph Lateral Scler Other Motor Neuron Disord, 1, p. S61.
12. Sen, I., Nalini, A., Joshi, N. B. and Joshi, P. G. (2005) Cerebrospinal fluid from amyotrophic lateral sclerosis patients preferentially elevates intracellular calcium and toxicity in motor neurons via AMPA/ kainate receptor. J Neurol Sci, 235, pp. 45-54.
13. Lin, C. I., Bristol, L. A., Jin, L., Dykes-Hoberg, M., Crawford, T. and Clawson, L. (1988) Aberrant RNA processing in a neurodegenerative disease: The cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron, 20, pp. 589-602.
14. Bendotti, C., Tortarolo, M., Suchak, S. K., Calvaresi, N., Carvelli, L. and Bastone, A. (2001) Transgenic SOD1 G93A mice develop reduced GLT-1 in spinal cord without alterations in cerebrospinal fluid glutamate levels. J Neurochem, 79, pp. 737-746.
15. Guo, H., Lai, L., Butchbach, M. E., Stockinger, M. P., Shan, X. and Bishop, G. A. (2003) Increased expression of the glial glutamate transporter EAAT2 modulates excitotoxicity and delays the onset but not the outcome of ALS in mice. Hum Mol Genet, 12, pp. 2519-2532.
16. Gurney, M. E., Cutting, F. B., Zhai, P., Doble, A., Taylor, C. P. and Andrus, P. K. (1996) Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Ann Neurol, 39, pp. 147-157.
17. Miller, R. G., Mitchell, J. D., Lyon, M. and Moore, D. H. (2003) Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Amyotroph Lateral Scler Other Motor Neuron Disord, 4, pp. 191-206.
18. Poloni, M., Facchetti, D., Mai, R., Micheli, A., Agnoletti, L. and Francolini, G. (2000) Circulating levels of tumor necrosis factor-a and its soluble receptors are increased in the blood of patients with amyotrophic lateral sclerosis. Neurosci Lett, 287, p. 2114.
19. Kawamata, T., Akiyama, H., Yamada, T. and McGeer, P. L. (1992) Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Pathol, 140, pp. 691-707.
20. Hall, E. D., Andrus, P. K., Oostveen, J. A., Fleck, T. J. and Gurney, M. E. (1998) Relationship of oxygen radical-induced lipid peroxidative damage to disease onset and progression in a transgenic model of familial ALS. J Neurosci, 53, pp. 66-77.
21. Olsen, M. K., Roberds, S. L., Ellerbrock, B. R., Fleck, T. J., McKinley, D. K. and Gurney, M. E. (2001) Disease mechanisms revealed by transcription profiling in SOD1-G93A transgenic mouse spinal cord. Ann Neurol, 50, pp. 730-740.
22. Hensley, K., Floyd, R. A., Gordon, B., Mou, S., Pye, Q. N. and Stewart, C. (2002) Temporal patterns of cytokine and apoptosis-related gene expression in spinal cords of the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. J Neurochem, 82, pp. 365-374.
23. Yoshihara, T., Ishigaki, S., Yamamoto, M., Liang, Y., Niwa, J. and Takeuchi, H. (2002) Differential expression of inflammation- and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem, 80, pp. 158-167.
24. Hensley, K., Fedynyshyn, J., Ferrell, S., Floyd, R. A., Gordon, B. and Grammas, P. (2003) Message and protein-level elevation of tumor necrosis factor a (TNFa) and TNFa-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis, 14, pp. 74-80.
25. Weydt, P., Weiss, M. D., Moller, T. and Carter, G. T. (2002) Neuro-inflammation as a therapeutic target in amyotrophic lateral sclerosis. Curr Opin Investig Drugs, 3, pp. 1720-1724.
26. Liu, B., Jiang, J. W., Wilson, B., Du, L., Yang, S. N. and Wang, J. Y. (2000) Systemic infusion of naloxone reduces degeneration of rat substantia nigral dopaminergic neurons induced by intranigral injection of lipopolysaccharide. J Pharmacol Exp Ther, 295, pp. 125-132.
27. Liu, B. and Hong, J. -S. (2003) Role of microgila in inflammation-mediated neurodegenerative diseases; mechanisms and strategies for therapeutic intervention. J Pharmacol Exper Ther, 304, pp. 1-7.
28. Liu, Y., Qin, L., Li, G., Zhang, W., An, L. and Liu, B. (2003) Dextromethorphan protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. J Pharmacol Exp Ther, 305, pp. 212-218.
29. Kriz, J., Nguyen, M. D. and Julien, J. P. (2002) Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis, 10, pp. 268-278.
30. Kriz, J., Gowing, G. and Julien, J. -P. (2003) Efficient three-drug cocktail for disease induced by mutant superoxide dismutase. Annal Neurol, 53, pp. 429-436.
31. Bosch, L. van den, Tilkin, P., Lemmens, G. and Robberecht, W. (2002) Minocycline delays disease onset and mortality in a transgenic model of ALS. Neuroreport, 13, pp. 1067-1070.
32. Zhang, W., Narayanan, M. and Friedlander, R. M. (2003) Additive neuroprotective effects of minocycline with creatine in a mouse model of ALS. Ann Neurol, 53, pp. 267-270.
33. West, M., Mhatre, M., Ceballos, A., Floyd, R. A., Grammas, P. and Gabbita, S. P. (2004) The arachidonic acid 5-lipoxygenase inhibitor nordihydroguaiaretic acid inhibits tumor necrosis factor a activation of microglia and extends survival of G93A-SOD1 transgenic mice. J Neurochem, 91, pp. 133-143.
34. Hirano, A., Nakano, I., Kurland, L. T., Mulder, D. W., Holley, P. W. and Saccomanno, G. (1984) Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J Neuropathol Exp Neurol, 43, pp. 471-480.
35. Hirano, A. (1991) Cytopathology of amyotrophic lateral sclerosis. Adv Neurol, 56, pp. 91-101.
36. Tomkins, J., Usher, P., Slade, J. Y., Ince, P. G., Curtis, A. and Bushby, K. (1998) Novel insertion in the KSP region of the neurofilament heavy gene in amyotrophic lateral sclerosis (ALS). Neuroreport, 9, pp. 3967-3970.
37. Al-Chalabi, A., Andersen, P. M., Nilsson, P., Chioza, B., Andersson, J. L. and Russ, C. (1999) Deletions of the heavy neurofilament subunit tail in amyotrophic lateral sclerosis. Hum Mol Genet, 8, pp. 157-164.
38. Bergeron, C., Beric-Maskarel, K., Muntasser, S., Weyer, L., Somerville, M. J. and Percy, M. E. (1994) Neurofilament light and polyadenylated mRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J Neuropathol Exp Neurol, 53, pp. 221-230.
39. Williamson, T. L., Bruijn, L. I., Zhu, Q., Anderson, K. L., Anderson, S. D. and Julien, J. P. (1998) 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, pp. 6931-6936.
40. Farah, C. A., Nguyen, M. D., Julien, J. P. and Leclerc, N. (2003) Altered levels and distribution of microtubule-associated proteins before disease onset in a mouse model of amyotrophic lateral sclerosis. J Neurochem, 84, pp. 77-86.
41. Corbo, M. and Hays, A. P. (1992) Peripherin and neurofilament protein coexist in spinal spheroids of motor neuron disease. J Neuropathol Exp Neurol, 51, pp. 531-537.
42. He, C. Z. and Hays, A. P. (2004) Expression of peripherin in ubiquinated inclusions of amyotrophic lateral sclerosis. J Neurol Sci, 217, pp. 47-54.
43. Gros-Louis, F., Lariviere, R., Gowing, G., Laurent, S., Camu, W. and Bouchard, J. P. (2004) A frameshift deletion in peripherin gene associated with amyotrophic lateral sclerosis. J Biol Chem, 279, pp. 45951-45956.
44. Leung, C. L., He, C. Z., Kaufmann, P., Chin, S. S., Naini, A. and Liem, R. K. (2004) A pathogenic peripherin gene mutation in a patient with amyotrophic lateral sclerosis. Brain Pathol, 14, pp. 290-296.
45. Beaulieu, J. M., Nguyen, M. D. and Julien, J. P. (1999) Late onset of motor neurons in mice overexpressing wild-type peripherin. J Cell Biol, 147, pp. 531-544.
46. Beaulieu, J. M. and Julien, J. P. (2003) Peripherin-mediated death of motor neurons rescued by overexpression of neurofilament NF-H proteins. J Neurochem, 85, pp. 248-256.
47. Williamson, T. L. and Cleveland, D. W. (1999) Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci, 2, pp. 50-56.
48. LaMonte, B. H., Wallace, K. E., Holloway, B. A., Shelly, S. S., Ascano, J. and Tokito, M. (2002) Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron, 34, pp. 715-727.
49. Wong, P. C., Pardo, C. A., Borchelt, D. R., Lee, M. K., Copeland, N. G. and Jenkins, N. A. (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron, 14, pp. 1105-1116.
50. Jaarsma, D., Rognoni, F., van Duijn, W., Verspaget, H. W., Haasdijk, E. D. and Holstege, J. C. (2001) Cu/Zn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol. (Berlin), 102, pp. 293-305.
51. Liu, J., Lillo, C., Jonsson, P. A., Velde, C. Vande, Ward, C. M. and Miller, T. M. (2004) Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron, 43, pp. 5-17.
52. Takeuchi, H., Kobayashi, Y., Ishigaki, S., Doyu, M. and Sobue, G. (2002) Mitochondrial localization of mutant superoxide dismutase 1 triggers caspase-dependent cell death in a cellular model of familial amyotrophic lateral sclerosis. J Biol Chem, 277, pp. 50966-50972.
53. Gunther, M. R., Vangilder, R., Fang, J. and Beattie, D. S. (2004) Expression of a familial amyotrophic lateral sclerosis-associated mutant human superoxide dismutase in yeast leads to decreased mitochondrial electron transport. Arch Biochem Biophys, 431, pp. 207-214.
54. Bruijn, L. I., Houseweart, M. K., Kato, S., Anderson, K. L., Anderson, S. D. and Ohama, E. (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science, 281, pp. 1851-1854.
55. Wang, J., Slunt, H., Gonzales, V., Fromholt, D., Coonfield, M. and Copeland, N. G. (2003) Copper-binding-site-null SOD1 causes ALS in transgenic mice: Aggregates of non-native SOD1 delineate a common feature. Hum Mol Genet, 12, pp. 2753-2764.
56. Son, M., Cloyd, C. D., Rothstein, J. D., Rajendran, B. and Elliott, J. L. (2003) Aggregate formation in Cu/Zn superoxide dismutase-related proteins. J Biol Chem, 278, pp. 14331-14336.
57. Wilczak, N., de Vos, R. A. I. and de Keyser, J. (2003) Free insulin-like growth factor (IGF)-1 and IGF binding proteins 2, 5 and 6 in spinal motor neurons in amyotrophic lateral sclerosis. Lancet, 361, pp. 1007-1011.
58. Kaspar, B. K., Llado, J., Sherkat, N., Rothstein, J. D. and Gage, F. H. (2003) Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science, 301, pp. 839-842.
59. Acsadi, G., Anguelov, R. A., Yang, H., Toth, G., Thomas, R. and Jani, A. (2002) Increased survival and function of SOD1 mice after glial cell-derived neurotrophic factor gene therapy. Hum Gene Ther, 13, pp. 1047-1059.
60. Azzouz, M., Ralph, G. S., Storkebaum, E., Walmsley, L. E., Mitrophanous, K. A. and Kingsman, S. M. (2004) VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature, 429, pp. 413-417.
61. Oosthuyse, B., Moons, L., Storkebaum, E., Beck, H., Nuyens, D. and Brusselmans, K. (2001) Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet, 28, pp. 131-138.
62. Li, M., Ona, V. O., Guegan, C., Chen, M., Jackson-Lewis, V. and Andrews, L. J. (2000) Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science, 288, pp. 335-339.
63. Inoue, H., Tsukita, K., Iwasato, T., Suzuki, Y., Tomioka, M. and Tateno, M. (2003) The crucial role of caspase-9 in the disease progression of a transgenic ALS mouse model. EMBO J, 22, pp. 6665-6674.
64. Kostic, V., Jackson-Lewis, V., de Bilbao, F., Dubois-Dauphin, M. and Przedborsk, I. S. (1997) Bcl-2: Prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science, 277, pp. 559-562.
65. Pasinelli, P., Belford, M. E., Lennon, N., Bacskai, B. J., Hyman, B. T. and Trotti, D. (2004) Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron, 43, pp. 19-30.
66. Sugawara, T., Lewen, A., Gasche, Y., Yu, F. and Chan, P. H. (2002) Overexpression of SOD1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release. FASEB J, 16, pp. 1997-1999.
67. Raoul, C., Estevez, A. G., Nishimune, H., Cleveland, D. W., de Lapeyriere, O. and Henderson, C. E. (2002) Motor neuron death triggered by a specific pathway downstream of fas: Potentiation by ALS-linked SOD1 mutations. Neuron, 35, pp. 1067-1083.
68. Dineley, K. E., Votyakova, T. V. and Reynolds, I. J. (2003) Zinc inhibition of cellular energy production: Implications for mitochondria and neurodegeneration. J Neurochem, 85, pp. 563-570.
69. Wiedau-Pazos, M., Goto, J. J., Rabizadeh, S., Gralla, E. B., Roe, J. A. and Lee, M. K. (1996) Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science, 271, pp. 515-518.
70. Estevez, A. G., Crow, J. P., Sampson, J. B., Reiter, C., Zhuang, Y. and Richardson, G. J. (1999) Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science, 286, pp. 2498-5000.
71. Crow, J. P., Sampson, J. B., Zhuang, Y., Thompson, J. A. and Beckman, J. S. (1997) Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J Neurochem, 69, pp. 1936-1944.
72. Kang, J. H. and Eum, W. S. (2000) Enhanced oxidative damage by the familial amyotrophic lateral sclerosis-associated Cu/Zn-superoxide dismutase mutants. Biochim Biophys Acta, 1524, pp. 162-170.
73. Rothstein, J. D. (1995) Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin Neurosci, 3, pp. 348-359.
74. Becher, B., Prat, A. and Antel, J. P. (2000) Brain-immune connection: immunoregulatory properties of CNS-resident cells. Glia, 29, pp. 293-304.
75. Allan, S. M. and Rothwell, N. J. (2001) Cytokines and acute neurodegeneration. Nature Revs Neurosci, 2, pp. 734-744.
76. Hanisch, U. K. (2000) Microglia as a source and target of cytokines. Glia, 40, pp. 140-155.
77. Couillard-Despres, S., Zhu, Q., Wong, P. C., Price, D. L., Cleveland, D. W. and Julien, J. P. (1998) Protective effect of neurofilament heavy gene overexpression in motor neuron disease induced by mutant superoxide dismutase. Proc Natl Acad Sci. USA, 95, pp. 9626-9630.
78. Kong, J. and Xu, Z. (2000) Overexpression of neurofilament subunit NF-L and NF-H extends survival of a mouse model for amyotrophic lateral sclerosis. Neurosci Lett, 281, pp. 72-74.
79. Xu, Z., Cork, L. C., Griffin, J. W. and Cleveland, D. W. (1993) Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell, 73, pp. 23-33.
80. Meier, J., Couillard-Despres, S., Jacomy, H., Gravel, C. and Julien, J. P. (1999) Extra neurofilament NF-L subunits rescue motor neuron disease caused by overexpression of the human NF-H gene in mice. J Neuropathol Exp Neurol, 58, pp. 1099-1100.
81. Kieran, D., Hafezparast, M., Bohnert, S., Dick, J. R. T., Martin, J. and Schiavo, G. (2005) A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J Cell Biol, 169, pp. 561-567.
82. Kabashi, E., Agar, J. N., Taylor, D. M., Minotti, S. and Durham, H. D. (2004) Focal dysfunction of the proteasome: A pathogenic factor in a mouse model of amyotrophic lateral sclerosis. J Neurochem, 89, pp. 1325-1335.
83. Bruening, W., Roy, J., Giasson, B., Figlewicz, D. A., Mushynski, W. E. and Durham, H. D. (1999) Up-regulation of protein chaperones preserves viability of cells expressing toxic Cu/Zn-superoxide dismutase mutants associated with amyotrophic lateral sclerosis. J Neurochem, 72, pp. 693-699.
84. Lai, E. C., Felice, K. J., Festoff, B. W., Gawel, M. J., Gelinas, D. F. and Kratz, R. (1997) Effect of recombinant human insulin-like growth factor-1 on progression of ALS: A placebo-controlled study. Neurology, 49, pp. 1621-1630.
85. Borasio, G. D., Robberecht, W., Leigh, P. N., Emile, J., Guiloff, R. J. and Jerusalem, F. (1998) A placebo-controlled trial of human insulin-like growth factor-1 on amyotrophic lateral sclerosis. Neurology, 51, pp. 583-586.
86. Zoratti, M. and Szabo, I. (1995) The mitochondrial permeability transition. Biochim Biophys Acta, 1241, pp. 139-176.
87. Jiang, D., Sullivan, P. G., Sensi, S. L., Steward, O. and Weiss, J. H. (2001) Zn(2+) induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. J Biol Chem, 276, pp. 47524-47529.
88. Volterra, A., Trotti, D., Tromba, C., Floridi, S. and Racagni, G. (1994) Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. J Neurosci, 14, pp. 2924-2932.
89. Christman, J. W., Blackwell, T. S. and Juurlink, B. H. J. (2000) Redox regulation of nuclear factor kappa B: Therapeutic potential for attenuating inflammatory responses. Brain Pathol, 10, pp. 153-162.
90. Buttket, T. M. and Sandstom, P. A. (1994) Oxidative stress as a mediator of apoptosis. Immunol Today, 15, pp. 7-10.
91. Colavitti, R., Pani, G., Bedogni, B., Anzevino, R., Borrello, S. and Waltenberger, J. (2002) Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/ KDR. J Biol Chem, 277, pp. 3101-3108.
92. Finkel, T. (1998) Oxygen radicals and signaling. Curr Opin Cell Biol, 10, pp. 248-253.
93. Cassina, P., Pehar, M., Vargas, M. R., Castellanos, R., Barbeito, A. G. and Estevez, A. G. (2005) Astrocyte activation by fibroblast growth factor-1 and motor neuron apoptosis: Implications for amyotrophic lateral sclerosis. J Neurochem, 93, pp. 38-46.
94. Kim, N. H. and Kang, J. H. (2003) Oxidative modification of neurofilament-L by copper-catalyzed reaction. J Biochem Mol Biol, 36, pp. 488-492.
95. Lafon-Cazal, M., Pietri, S., Culcasi, M. and Bockaert, J. (1993) NMDA-dependent superoxide production and neurotoxicity. Nature, 364, pp. 535-537.
96. Kreutzberg, G. W. (1996) Microglia: A sensor for pathological events in the CNS. Trends Neurosci, 19, pp. 312-318.
97. Ankarcrona, M., Dypbukt, J. M., Bonfoco, E., Zhivotovsky, B., Orrenius, S. and Lipton, S. A. (1995) Glutamate-induced neuronal death: A succession of necrosis or apoptosis depending on mitochondrial function. Neuron, 15, pp. 961-973.
98. Chung, R. S., McCormack, G. H., King, A. E., West, A. K. and Vickers, J. C. (1995) Glutamate induces rapid loss of axonal neurofilament proteins from cortical neurons in vitro. Exp Neurol, 193, pp. 481-488.
99. Tarabal, O., Caldero, J., Casas, C., Oppenheim, R. W. and Esquerda, J. E. (2005) Protein retention in the endoplasmic reticulum, blockade of programmed cell death and autophagy selectively occur in spinal cord motor neurons after glutamate receptor-mediated injury. Mol Cell Neurosci, 29, pp. 283-298.
100. Choi, J. S., Kim, S. Y., Park, H. J., Cha, J. H., Choi, Y. S. and Chung, J. W. (2004) Differential regulation of ciliary neurotrophic factor and its receptor in the rat hippocampus in response to kainic acid-induced excitotoxicity. Mol Cells, 17, pp. 292-296.
101. Colton, C. A., Snell, J., Chernyshev, O. and Gilbert, D. L. (1994) Induction of superoxide anion and nitric oxide production in cultured microglia. Ann N.Y. Acad Sci, 738, pp. 54-63.
102. Tikka, T., Fiebich, B. L., Goldsteins, G., Keinanen, R. and Koistinaho, J. (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci, 21, pp. 2580-2588.
103. Turpaev, K., Litvinov, D., Dubovaya, V., Panasyuk, A., Ivanov, D. and Prassolov, V. (2001) Induction of vascular endothelial growth factor by nitric oxide in cultured human articular chondrocytes. Biochimie, 83, pp. 515-522.
104. Rempel, H., Kusdra, L. and Pulliam, L. (2001) Interleukin-1b up-regulates expression of neurofilament light in human neuronal cells. J Neurochem, 78, pp. 640-645.
105. Emerit, J., Edeas, M. and Bricaire, F. (2004) Neurodegenerative diseases and oxidative stress. Biomed Pharmacother, 58, pp. 39-46.
106. Grzenkowicz-Wydra, J., Cisowski, J., Nakonieczna, J., Zarebski, A., Udilova, N. and Nohl, H. (2004) Gene transfer of Cu/Zn superoxide dismutase enhances the synthesis of vascular endothelial growth factor. Mol Cell Biochem, 264, pp. 169-181.
107. Escartin, C., Boyer, F., Bemelmans, A. P., Hantraye, P. and Brouillet, E. (2004) Insulin growth factor-1 protects against excitotoxicity in the rat striatum. Neuroreport, 15, pp. 2251-2254.
108. Schuettauf, F., Vorwerk, C., Naskar, R., Orlin, A., Quinto, K. and Zurakowski, D. (2004) Adeno-associated viruses containing bFGF or BDNF are neuroprotective against excitotoxicity. Curr Eye Res, 29, pp. 379-386.
109. Tseng, H. C. and Dichter, M. A. (2005) Platelet-derived growth factor-BB pretreatment attenuates excitotoxic death in cultured hippocampal neurons. Neurobiol Dis, 19, pp. 77-83.
110. Kitagawa, A., Nakayama, T., Takenaga, M., Matsumoto, K., Tokura, Y. and Ohta, Y. (2005) Lecithinized brain-derived neurotrophic factor promotes the differentiation of embryonic stem cells in vitro and in vivo. Biochem Biophys Res Commun, 328, pp. 1051-1057.
111. Borchelt, D. R., Guarnieri, M., Wong, P. C., Lee, M. K., Slunt, H. S. and Xu, Z. S. (1995) Superoxide dismutase 1 subunits with mutations linked to familial amyotrophic lateral sclerosis do not affect wild-type subunit function. J Biol Chem, 270, pp. 3234-3238.
112. Reaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J. and Siwek, D. F. (1996) Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat Genet, 13, pp. 43-47.
113. Bruijn, L. I. and Cleveland, D. W. (2004) Unravelling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci, 27, pp. 723-749.
114. Bruijn, L. I., Beal, M. F., Becher, M. W., Schulz, J. B., Wong, P. C. and Price, D. L. (1997) Elevated free nitrotyrosine levels, but not protein-bound nitrotyrosine or hydroxyl radicals, throughout amyotrophic lateral sclerosis (ALS)-like disease implicate tyrosine nitration as an aberrant in vivo property of one familial ALS-linked superoxide dismutase 1 mutant. Proc Natl Acad Sci. USA, 94, pp. 7606-7611.
115. Forman, H. J. and Fridovich, I. (1973) On the stability of bovine superoxide dismutase. The effects of metals. J Biol Chem, 248, pp. 2645-2649.
116. Goto, J. J., Zhu, H., Sanchez, R. J., Nersissian, A., Gralla, E. B. and Valentine, J. S. (2000) Loss of in vitro metal ion binding specificity in mutant copper-zinc superoxide dismutases associated with familial amyotrophic lateral sclerosis. J Biol Chem, 275, pp. 1007-1014.
117. Subramaniam, J. R., Lyons, W. E., Liu, J., Bartnikas, T. B., Rothstein, J. D. and Price, D. L. (2002) Mutant SOD1 causes motor neuron disease independent of copper chaperone-mediated copper loading. Nat Neurosci, 5, pp. 301-307.
118. Elliott, J. L. (2001) Zinc and copper in the pathogenesis of amyotrophic lateral sclerosis. Prog Neuro-Psychopharmacol & Biol Psychiat, 25, pp. 1169-1185.
119. Lyons, T. J., Liu, H., Goto, J. J., Nersissian, A., Roe, J. A. and Graden, J. A. (1996) Mutations in copper-zinc superoxide dismutase that cause amyotrophic lateral sclerosis alter the zinc binding site and the redox behavior of the protein. Proc Natl Acad Sci. USA, 93, pp. 12240-12244.
120. Rodriguez, J. A., Valentine, J. S., Eggers, D. K., Roe, J. A., Tiwari, A. and Brown, R. H Jr. (2002) Familial amyotrophic lateral sclerosis-associated mutations decrease the thermal stability of distinctly metallated species of human copper/zinc superoxide dismutase. J Biol Chem, 277, pp. 15932-15937.
121. Williamson, T. L., Corson, L. B., Huang, L., Burlingame, M., Liu, J. and Bruijn, L. I. (2000) Toxicity of ALS-linked SOD1 mutants. Science, 286, pp. 2498-2500.
122. Noh, K. M., Kim, Y. H. and Koh, J. Y. (1999) Mediation by membrane protein kinase C of zinc-induced oxidative neuronal injury in mouse cortical cultures. J Neurochem, 72, pp. 1609-1616.
123. Persechini, A., McMillan, K. and Masters, B. S. (1995) Inhibition of nitric oxide synthase activity by Zn2+ ion. Biochemistry, 34, pp. 15091-15095.
124. Oteiza, P. I., Olin, K. L., Fraga, C. G. and Keen, C. L. (1995) Zinc deficiency causes oxidative damage to proteins, lipids and DNA in rat testes. J Nutr, 125, pp. 823-829.
125. Bray, T. M. and Bettger, W. J. (1990) The physiological role of zinc as an antioxidant. Free Radic Biol Med, 8, pp. 281-291.
126. Chen, N., Moshaver, A. and Raymond, L. A. (1997) Differential sensitivity of recombinant N-methyl-D-aspartate receptor subtypes to zinc inhibition. Mol Pharmacol, 51, pp. 1015-1023.
127. Sensi, S. L. and Jeng, J. M. (2004) Re-thinking the excitotoxic ionic milieu: The emerging role of zinc in ischemic neuronal injury. Curr Mol Med, 4, pp. 83-107.
128. Westbrook, G. L. and Mayer, M. L. (1987) Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature, 328, pp. 640-643.
129. Harrison, N. L., Radke, H. K., Talukder, G. and French-Mullen, J. M. (1993) Zinc modulates transient outward current gating in hippocampal neurons. Receptors Channels, 1, pp. 153-163.
130. Raman, C. S., Li, H., Martasek, P., Kral, V., Masters, B. S. and Poulos, T. L. (1998) Crystal structure of constitutive endothelial nitric oxide synthase: A paradigm for pterin function involving a novel metal center. Cell, 95, pp. 939-950.
131. Ghosh, D. K., Crane, B. R., Ghosh, S., Wolan, D., Gachhui, R. and Crooks, C. (1999) Inducible nitric oxide synthase: Role of the N-terminal beta-hairpin hook and pterin-binding segment in dimerization and tetrahydrobiopterin interaction. EMBO J, 18, pp. 6260-6270.
132. Ge, W. W., Wen, W., Strong, W., Leystra-Lantz, C. and Strong, M. J. (2005) Mutant copper-zinc superoxide dismutase binds to and destabilizes human low molecular weight neurofilament mRNA. J Biol Chem, 280, pp. 118-124.
133. Lorusso, M., Cocco, T., Sardanelli, A. M., Minuto, M., Bonomi, F. and Papa, S. (1991) Interaction of Zn2+ with the bovine-heart mitochondrial bc1 complex. Eur J Biochem, 197, pp. 555-561.
134. Brown, A. M., Kristal, B. S., Effron, M. S., Shestopalov, A. I., Ullucci, P. A. and Sheu, K. F. (2000) Zn2+ inhibits alpha-ketoglutarate-stimulated mitochondrial respiration and the isolated alpha-ketoglutarate dehydrogenase complex. J Biol Chem, 275, pp. 13441-13447.
135. Maret, W., Yetman, C. A. and Jiang, L. (2001) Enzyme regulation by reversible zinc inhibition: Glycerol phosphate dehydrogenase as an example. Chem Biol Interact, 130, pp. 891-901.
136. Gazaryan, I. G., Krasnikov, B. F., Ashby, G. A., Thorneley, R. N., Kristal, B. S. and Brown, A. M. (2002) Zinc is a potent inhibitor of thiol oxidoreductase activity and stimulates reactive oxygen species production by lipoamide dehydrogenase. J Biol Chem, 277, pp. 10064-10072.
137. Rakhit, R., Cunningham, P., Furtos-Matei, A., Dahan, S., Qi, X. F. and Crow, J. P. (2002) Oxidation-induced misfolding and aggregation of superoxide dismutase and its implications for amyotrophic lateral sclerosis. J Biol Chem, 277, pp. 47551-47556.
138. Sampson, J. B. and Beckman, J. S. (2001) Hydrogen peroxide damages the zinc-binding site of zinc-deficient Cu/Zn superoxide dismutase. Arch Biochem Biophys, 392, pp. 8-13.
139. Curtain, C. C., Ali, F., Volitakis, I., Cherny, R. A., Norton, R. S. and Beyreuther, K. (2001) Alzheimer's disease amyloid-beta binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits. J Biol Chem, 276, pp. 20466-20473.
140. Quaglio, E., Chiesa, R. and Harris, D. A. (2001) Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J Biol Chem, 276, pp. 11432-11438.
141. Yu, Z. P., Le, G. W. and Shi, Y. H. (2005) Effect of zinc sulphate and zinc methionine on growth, plasma growth hormone concentration, growth hormone receptor and insulin-like growth factor-1 gene expression in mice. Clin Exp Pharmacol Physiol, 32, pp. 273-278.
142. Kwon, H. S., Shin, H. C. and Kim, J. S. (2005) Suppression of vascular endothelial growth factor expression at the transcriptional and post-transcriptional levels. Nucleic Acids Res, 33, p. 74.
143. Ciais, D., Cherradi, N., Bailly, S., Grenier, E., Berra, E. and Pouyssegur, J. (2004) Destabilization of vascular endothelial growth factor mRNA by the zinc-finger protein TIS11b. Oncogene, 23, pp. 8673-8680.
144. Kuramoto, K., Uesaka, T., Kimura, A., Kobayashi, M. H. W. and Katoh, O. (2000) ZK7, a novel zinc finger gene, is induced by vascular endothelial growth factor and inhibits apoptotic death in hematopoietic cells. Cancer Res, 60, pp. 425-430.
145. Woodbury, D., Schaar, D. G., Ramakrishnan, L. and Black, I. B. (1998) Novel structure of the human GDNF gene. Brain Res, 803, pp. 95-104.
146. Yajima, S., Lammers, C. H., Lee, S. H., Hara, Y., Mizuno, K. and Mouradian, M. M. (1997) Cloning and characterization of murine glial cell-derived neurotrophic factor inducible transcription factor (MGIF). J Neurosci, 17, pp. 8657-8666.
147. Uzzo, R. G., Leavis, P., Hatch, W., Gabai, V. L., Dulin, N. and Zvartau, N. (2002) Zinc inhibits nuclear factor-kappa B activation and sensitizes prostate cancer cells to cytotoxic agents. Clin Cancer Res, 8, pp. 3579-3583.
148. Schott-Ohly, P., Lgssiar, A., Partke, H. J., Hassan, M., Friesen, N. and Gleichmann, H. (2004) Prevention of spontaneous and experimentally induced diabetes in mice with zinc sulfate-enriched drinking water is associated with activation and reduction of NF-kappa B and AP-1 in islets, respectively. Exp Biol Med. (Maywood), 229, pp. 1177-1185.
149. Maire, M. A., Rast, C., Pagnout, C. and Vasseu, R. P. (2004) Changes in expression of bcl-2 and bax in Syrian hamster embryo (SHE) cells exposed to ZnCl(2). Arch Toxicol, 79, pp. 90-101.
150. Iitaka, M., Kakinuma, S., Fujimaki, S., Oosuga, I., Fujita, T. and Yamanaka, K. (2001) Induction of apoptosis and necrosis by zinc in human thyroid cancer cell lines. J Endocrinol, 169, pp. 417-424.
151. Hainaut, P. and Mann, K. (2001) Zinc binding and redox control of p53 structure and function. Antioxid Redox Signal, 3, pp. 611-623.
152. Frederickson, C. J., Suh, S. W., Silva, D., Frederickson, C. J. and Thompson, R. B. (2000) Importance of zinc in the central nervous system: the zinc-containing neuron. J Nutr, 130, p. S147.
153. Hidalgo, J., Aschner, M., Zatta, P. and Vasak, M. (2001) Roles of the metallothionein family of proteins in the central nervous system. Brain Res Bull, 55, pp. 133-145.
154. Vela, J. M., Hidalgo, J., Gonzalez, B. and Castellano, B. (1997) Induction of metallothionein in astrocytes and microglia in the spinal cord from the myelin-deficient jimpy mouse. Brain Res, 767, pp. 345-355.
155. Acarin, L., Gonzalez, B., Hidalgo, J., Castro, A. J. and Castellano, B. (1999) Primary cortical glial reaction versus secondary thalamic glial response in the excitotoxically injured young brain: Astroglial response and metallothionein expression. Neuroscience, 92, pp. 827-839.
156. Carrasco, J., Giralt, M., Molinero, A., Penkowa, M., Moos, T. and Hidalgo, J. (1999) Metallothionein (MT)-III: Generation of polyclonal antibodies, comparison with MT-I+II in the freeze lesioned rat brain and in a bioassay with astrocytes, and analysis of Alzheimer's disease brains. J Neurotrauma, 16, pp. 1115-1129.
157. Carrasco, J., Penkowa, M., Hadberg, H., Molinero, A. and Hidalgo, J. (2000) Enhanced seizures and hippocampal neurodegeneration following kainic acid-induced seizures in metallothionein-I+II-deficient mice. Eur J Neurosci, 12, pp. 2311-2322.
158. Carrasco, J., Giralt, M., Penkowa, M., Stalder, A. K., Campbell, I. L. and Hidalgo, J. (2000) Metallothioneins are up-regulated in symptomatic mice with astrocyte-targeted expression of tumor necrosis factor-alpha. Exp Neurol, 163, pp. 46-54.
159. Hamer, D. H. (1986) Metallothionein. Annu Rev Biochem, 55, pp. 913-951.
160. Hager, I. J. and Palmiter, R. D. (1981) Transcriptional regulation of mouse liver metallothionein-I gene by glucocorticoids. Nature, 291, pp. 340-342.
161. Hozumi, I., Inuzuka, T., Hiraiwa, M., Uchida, Y., Anezaki, T. and Ishiguro, H. (1995) Changes of growth inhibitory factor after stab wounds in rat brain. Brain Res, 688, pp. 143-148.
162. Dalton, T., Pazdernik, T. L., Wagner, J., Samson, F. and Andrews, G. K. (1995) Temporospatial patterns of expression of metallothionein-I and III and other stress-related genes in brain after kainic acid-induced seizures. Neurochem Int, 27, pp. 59-71.
163. Penkowa, M. and Moos, T. (1995) Disruption of the blood-brain interface in neonatal rat neocortex induces a transient expression of metallothionein in reactive astrocytes. Glia, 13, pp. 217-227.
164. Kim, E. H., Kim, T. S., Sun, W., Kim, D. S., Chung, H. S. and Kim, D. K. (2004) Differential regulation of metallothionein-I and metallothionein-II mRNA expression in the rat brain following traumatic brain injury. Mol Cells, 18, pp. 326-331.
165. Penkowa, M., Giralt, M., Thomsen, P. S., Carrasco, J. and Hidalgo, J. (2001) Zinc or copper deficiency-induced impaired inflammatory response to brain trauma may be caused by the concomitant metallothionein changes. J Neurotrauma, 18, pp. 447-463.
166. Erickson, J. C., Hollopeter, G., Thomas, S. A., Froelick, G. J. and Palmiter, R. D. (1997) Disruption of the metallothionein-III gene in mice: Analysis of brain zinc, behavior, and neuron vulnerability to metals, aging, and seizures. J Neurosci, 17, pp. 1271-1281.
167. Cole, T. B., Robbins, C. A., Wenzel, H. J., Schwartzkroin, P. A. and Palmiter, R. D. (2000) Seizures and neuronal damage in mice lacking vesicular zinc. Epilepsy Res, 39, pp. 153-169.
168. Gong, Y. H. and Elliott, J. L. (2000) Metallothionein expression is altered in a transgenic murine model of familial amyotrophic lateral sclerosis. Exp Neurol, 162, pp. 27-36.
169. Ignacio, S., Moore, D. H., Smith, A. P. and Lee, N. M. (2005) Effect of neuroprotective drugs on gene expression in G93A/SOD1 mice. Ann NY Acad Sci, 1053, pp. 121-136.
170. Nagano, S., Satoh, M., Sumi, H., Fujimura, H., Tohyama, C. and Yanagihara, T. (2001) Reduction of metallothioneins promotes the disease expression of familial amyotrophic lateral sclerosis mice in a dose-dependent manner. Eur J Neurosci, 13, pp. 1363-1370.
171. Puttaparthi, K., Gitomer, W. L., Krishnan, U., Son, M., Rajendran, B. and Elliott, J. L. (2002) Disease progression in a transgenic model of familial amyotrophic lateral sclerosis is dependent on both neuronal and non-neuronal zinc-binding proteins. J Neurosci, 22, pp. 8790-8796.
172. Smitt, P. A. Sillevis, Blaauwgeers, H. G., Troost, D. and de Jong, J. M. (1992) Metallothionein immunoreactivity is increased in the spinal cord of patients with amyotrophic lateral sclerosis. Neurosci Lett, 144, pp. 107-110.
173. Blaauwgeers, H. G., Chand, M. Anwar, Berg, F. M. van den, de Jong, J. M. Vianney and Troost, D. (1996) Expression of different metallothionein messenger ribonucleic acids in motor cortex, spinal cord and liver from patients with amyotrophic lateral sclerosis. J Neurol Sci, 142, pp. 39-44.
174. Liuzzi, J. P. and Cousins, R. P. (2004) Mammalian zinc transporters. Annu Rev Nutr, 24, pp. 151-172.
175. Sekler, I., Moran, A., Hershfinkel, M., Dori, A., Margulis, A. and Birenzweig, N. (2002) Distribution of the zinc transporter ZnT-1 compared with chelatable zinc in the mouse brain. J Comp Neurol, 447, pp. 201-209.
176. Wenzel, H. J., Cole, T. B., Born, D. E., Schwartzkroin, P. A. and Palmiter, R. D. (1997) Ultrastructural localization of zinc transporter-3 (ZnT-3) to synaptic vesicle membranes within mossy fiber boutons in the hippocampus of mouse and monkey. Proc Natl Acad Sci. USA, 94, pp. 12676-12681.
177. Nolte, C., Gore, A., Sekler, I., Kresse, W., Hershfinkel, M. and Hoffmann, A. (2004) ZnT-1 expression in astroglial cells protects against zinc toxicity and slows the accumulation of intracellular zinc. Glia, 148, pp. 145-155.
178. Segal, D., Ohana, E., Besser, L., Hershfinkel, M., Moran, A. and Sekler, I. (2004) A role for ZnT-1 in regulating cellular cation influx. Biochem Biophys Res Commun, 323, pp. 1145-1150.
179. Devergnas, S., Chimienti, F., Naud, N., Pennequin, A., Coquerel, Y. and Chantegrel, J. (2004) Differential regulation of zinc efflux transporters ZnT-1, ZnT-5 and ZnT-7 gene expression by zinc levels: A real time RT-PCR study. Biochem Pharmacol, 68, pp. 699-709.
180. Wang, F., Dufner-Beattie, J., Kim, B. E., Petris, M. J., Andrews, G. K. and Eide, D. J. (2004) Zinc-stimulated endocytosis controls activity of the mouse Zip1 and Zip3 zinc uptake transporters. J Biol Chem, 279, pp. 24631-24639.
181. Lovell, M. A., Smith, J. L., Xiong, S. and Markesbery, W. R. (2005) Alterations in zinc transporter protein-1 (ZnT-1) in the brain of subjects with mild cognitive impairment, early, and late-stage Alzheimer's disease. Neurotox Res.7, pp. 265-271.
182. Friedlich, A. L., Lee, J. -Y., van Groen, T., Cherny, R. A., Volitakis, I. and Cole, T. B. (2004) Neuronal zinc exchange with the blood vessel wall promotes cerebral amyloid angiopathy in an animal model of Alzheimer's disease. J Neurosci, 24, pp. 3453-3459.
183. Varshney, U., Hoar, D. I., Starozik, D. and Gedamu, L. (1984) A frequent restriction fragment length polymorphism in the human metallothionein-II processed gene region is evolutionarily conserved. Mol Biol Med, 2, pp. 193-206.
184. Morahan, J. M., Yu, B., Trent, R. J. and Pamphlett, R. (2005) Screening the metallothionein III gene in sporadic amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord, 6, pp. 115-117.
185. Cragg, R. A., Christie, G. R., Phillips, S. R., Russi, R. M., Kury, S. and Mathers, J. C. (2002) A novel zinc-regulated human zinc transporter, hZTL1, is localized to the enterocyte Ap6cal membrane. J Biol Chem, 277, pp. 22789-22797.
186. Nishimura, A. L., Mitne-Neto, M., Silva, H. C., Richieri-Costa, A., Middleton, S. and Cascio, D. (2004) A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am J Hum Genet, 75, pp. 822-831.
187. Cox, P. A., Banack, S. A. and Murch, S. J. (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci. USA, 100, pp. 13380-13383.
188. Armon, C. (2004) Excess incidence of ALS in young Gulf War veterans. Neurology, 63, pp. 1986-1987.