The roles of free radicals in amyotrophic lateral sclerosis: Reactive oxygen species and elevated oxidation of protein, DNA, and membrane phospholipids

FASEB Journal

Volumn 13, Issue 15, 1999, Pages 2318-2328

  Liu, Danxia ^a   Wen, Jing ^a   Liu, Jing ^a   Li, Liping ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Hydrogen peroxide; Hydroxyl radical; Mutation of Cu; Superoxide anion; Transgenic mouse; Zn superoxide dismutase gene

Indexed keywords

2,3 DIHYDROXYBENZOIC ACID; CELL DNA; CELL PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; DEOXYGUANOSINE DERIVATIVE; GENTISIC ACID; HYDROGEN PEROXIDE; HYDROXYL RADICAL; MALONALDEHYDE; MEMBRANE PHOSPHOLIPID; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVITY; GENE MUTATION; LIPID PEROXIDATION; MICRODIALYSIS; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SPINAL CORD;

EID: 0032764587     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.13.15.2318     Document Type: Article

References (66)

1. Rowland, L. P. (1995) Hereditary and acquired motor neuron disease. In Merritt's Textbook of Neurology (Rowland, L. P., ed) pp. 742-749, William & Wilkins, Philadelphia
2. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J. P., Deng, H-X., Rahmani, Z., Krizus, A., McKenna-Yasek, D., Cayabyab, A., Gaston, S. M., Berger, R., Tanzi, R. E., Halperin, J. J., Herzfeldt, B., Van den Bergh, R., Hung, W-Y., Bird, T., Deng, G., Mulder, D. W., Smyth, C., Laing, N. G., Soriano, E., Pericak-Vance, M. A., Haines, J., Rouleau, G. A., Gusella, J. S., Horvitz, H. R., and Brown, R. H., Jr. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature (London) 362, 59-62
3. Deng, H-X., Hentati, A., Tainer, J. A., Iqbal, Z., Cayabyab, A., Hung, W-Y., Getzoff, E. D., Hu, P., Herzfeldt, B., Roos, R. P., Warner, C., Deng, G., Soriano, E., Smyth, C., Parge, H. E., Ahmed, A., Roses, A. D., Hallewell, R. A., Pericak-Vance, M. A., and Siddique, T. (1993) Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 261, 1047-1051
4. Olanow, C. W. (1993) Superoxide dismutase and ALS. Trends Neurosci. 16, 439-444
5. Gurney, M. E., Pu, H., Chiu, A. Y., Canto, M. C. D., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H-X., Chen, W., Zhai, P., Sufit, R. L., and Siddique, T. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775
6. Siddique, T., and Deng, H-X. (1996) Genetic of amyotrophic lateral sclerosis. Hum. Mol. Genet. 5, 1465-1470
7. Belleroche, J., Orrell, R. W., and Virgo, L. (1996) Amyotrophic lateral sclerosis: recent advances in understanding disease mechanisms. J. Neuropathol. Exp. Neurol. 55, 747-757
8. Bowling, A. C., Schulz, J. B., Brown, R. H., Jr., and Beal, M. F. (1993) Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis. J. Neurochem. 61, 2322-2325
9. Iwasaki, I., Ikeda, K., and Kinoshita, M. (1993) Decreased cerebrospinal-fluid superoxide dismutase in amyotrophic lateral sclerosis. Lancet 342, 1118
10. Robberecht, W., Sapp, P., Viaene, M. K., Rosen, D., McKenna-Yasek, D., Haines, J., Horvitz, R., Theys, P., and Brown, R. H., Jr. (1994) Cu/Zn superoxide dismutase activity in familial and sporadic amyotrophic lateral sclerosis. J. Neurochem. 62, 384-387
11. Przedborski, S., Donaldson, D. M., Murphy, P. L., Hirsch, O., Lange, D. N., McKenna-Yasek, A. B., and Brown, R. H., Jr. (1996) Blood superoxide dismutase, catalase and glutathione peroxidase activities in familial and sporadic amyotrophic lateral sclerosis. Neurodegeneration 5, 57-64
12. Halliwell, B. (1989) Oxidants and the central nervous system, some fundamental questions. Is oxidant damage relevant to Parkinson's disease, Alzheimer's disease, traumatic injury or stroke? Acta Neurol Scand. 126, 23-33
13. Bergeron, C., Muntasser, S., Somerville, M. J., Weyer, L., and Percy, M. E. (1994) Copper/zine superoxide dismutase mRNA levels are increased in sporadic amyotrophic lateral sclerosis motoneurons. Brain Res. 659, 272-276
14. Yim, M. B., Chock, P. B., and Stadtman, E. R. (1990) Copper, zinc superoxide dismutase catalyzes hydroxyl radical production from hydrogen peroxide. Proc. Nail. Acad. Sci. USA 87, 5006-5010
15. Yim, M. B., Chock, P. B., and Stadtman, E. R. (1993) Enzyme function of copper, zinc superoxide dismutase as a free radical generator. J. Biol. Chem. 268, 4099-4105
16. m, for hydrogen peroxide. Proc. Natl. Acad. Sci. USA 93, 5709-5714
17. Wiedau-Pazos, M., Goto, J. J., Rabizadeh, S., Gralla, E. B., Roe, J. A., Lee, M. K., Valentine, J. S., and Bredesen, D. E. (1996) Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science 271, 515-520
18. m for hydrogen peroxide. J. Biol. Chem. 272, 8861-8863
19. Bruijn, L. I., Houseweart, M. K., Kato, S., Anderson, K. L., Anderson, S. D., Ohama, E., Reaume, A. G., Scott, R. W., and Cleveland, D. W. (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281, 1851-1854
20. Bruijn, L. I., Beal, M. F., Becher, M. W., Schulz, J. B., Wong, P. C., Price, D. L., and Cleveland, D. W. (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, 7606-7611
21. Liu, D., Wen, J., and Liu, J. (1998) Free radicals and oxidation in amyotrophic lateral sclerosis. J. Neurochem. 70, S7A (abstr.)
22. Bogdanov, M. B., Ramos, L. E., Xu, Z., and Beal, M. F. (1998) Elevated 'hydroxyl radical' generation in vivo in an animal model of amyotrophic lateral sclerosis. J. Neurochem. 71, 1321-1324
23. 2 Proc. Natl. Acad. Sci. USA 95, 6675-6680
24. Halliwell, B. (1987) Oxidants and human disease: some new concepts. FASEB J. 1, 358-364
25. Watson, B. D., and Ginsberg M. D. (1989) Ischemic injury in the brain. Role of oxygen radical-mediated processes. Ann. N.Y. Acad. Sci. 559, 269-281
26. Floyd, R. A., and Carney, J. M. (1992) Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann. Neurol. 32, S22-S27
27. Stadtman, E. R., and Oliver, C. N. (1991) Metal-catalyzed oxidation of proteins. J. Biol. Chem. 266, 2005-2008
28. Imlay, J. A., and Linn, S. (1988) DNA damage and oxygen radical toxicity. Science 240, 1302-1309
29. Marklund, S. L., Andersen, P. M., Forsgren, L., Nilsson, P., Ohlsson, P. I., Wikander, G., and Oberg, A. (1997) Normal binding and reactivity of copper in mutant superoxide dismutase isolated from amyotrophic lateral sclerosis patients. J. Neurochem. 69, 675-681
30. Ferrante, R. J., Browne, S. E., Shinobu, L. A., Bowling, A. C., Baik, M. J., MacGarvey, U., Kowall, N. W., Brown, R. H., Jr., and Beal, M. F. (1997) Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J. Neurochem. 69, 2064-2074
31. Ferrante, R. J., Shinobu, L. A., Schulz, J. B., Matthews, R. T., Thomas, C. E., Kowall, N. W., Gurney, M. E., and Beal, M. F. (1997) Increased 3-nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Ann. Neurol. 42, 326-334
32. 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. Res. 53, 66-77
33. Gurney, M. E., Curring, F. B., Zhai, P., Doble, A., Taylor, C. P., Andrus, P. K., and Hall, E. D. (1996) Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Ann. Neurol. 39, 147-157
34. Fitxmaurice, P. S., Shaw, I. C., Kleiner, H. E., Miller, R. T., Monks, T. J., Lau, S. S., Mitchell, J. D., and Lynch, P. G. (1996) Evidence for DNA damage in amyotrophic lateral sclerosis. Muscle Nerve 19, 797-798
35. Andrus, P., Fleck, T. J., Gurney, M. E., and Hall, E. D. (1998) Protein oxidative damage in a transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 71, 2041-2048
36. Liu, D., and McAdoo, D. J. (1993) Methylprcdnisolone reduces excitatory amino acid release following experimental spinal cord injury. Brain Res. 609, 293-297
37. Liu, D., and McAdoo, D. J. (1993) An experimental model combining microdialysis with electrophysiology, histology, and neurochemistry for exploring mechanisms of secondary damage in spinal cord injury: the effect of potassium. J. Neurotrauma 10, 349-362
38. Marsala, M., Malmberg, A. B., and Yaksh, T. L. (1995) The spinal loop dialysis catheter. Characterisation of use in the unanesthetised rat. J. Neurosci. Methods 62, 43-53
39. Liu, D. (1994) An experimental model combining microdialysis with electrophysiology, histology, and neurochemistry for studying excitotoxicity in spinal cord injury: effect of NMDA and kainate. Mol. Chem. Neuropathol. 23, 77-92
40. Liu, D., Sybert, T. E., Qian, H., and Liu, J. (1998) Superoxide production after spinal injury detected by microperfusion of cytochrome c. Free Rad. Biol, Med. 25, 298-304
41. Floyd, R. A., Watson, J. J., and Wong, P. K. (1984) Sensitive assay of hydroxyl free radical formation using high pressure liquid chromatography with electrochemical detection of phenol and salicylate hydroxylation products. J. Biochem. Biophys. Methods 10, 221-235
42. Floyd, R. A., Henderson, R., Watson, J. J., and Wong, P. K. (1986) Use of salicylate with high pressure liquid chromatography and electrochemical detection (LCED) as a sensitive measure of hydroxyl free radicals in adriamycin treated rats. Free Rad. Biol. Med. 2, 13-18
43. Liu, D., Liu, J., and Wen, J. Elevation of hydrogen peroxide after spinal cord injury detected by using the Fenton reaction. Free Rad. Biol. Med. 27, 478-482
44. Ingelman-Sundberg, M., Kaur, H., Terelius, Y., Persson, J.-O., and Halliwell, B. (1991) Hydroxylation of salicylate by microsomal fractions and cytochrome P-450. Biochem. J. 276, 753-757
45. Uchiyama, M., and Mihara, M. (1978) Determination of malondialdehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem. 86, 271-278
46. Ohkawa, H., Ohishi, N., and Yagi, K. (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351-358
47. Qian, H., and Liu, D. (1997) The lime course of malondialdehyde production following impact injury to rat spinal cord as measured by microdialysis and high pressure liquid chromatography. Neurochem. Res. 22, 1231-1236
48. Amici, A., Levine, R. L., Tsai, L., and Stadtman, E. R. (1989) Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions. J. Biol. Chem. 264, 3341-3349
49. Beland, F. A., Dooley, K. L., and Casciano, D. A. (1979) Rapid isolation of carcinogen-bound DNA and RNA by hydroxyapatite chromatography. J. Chromatogr. 174, 177-186
50. Levine, R. L., Garland, D., Oliver, C. N., Amici, A., Climent, I., Lenz, A.-G., Ahn, B.-W., Shaltiel, S., and Stadtman, E. R. (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186, 464-478
51. Floyd, R. A., Watson, J. J., Harris, J., West, M., and Wong, P. K. (1986) Formation of 8-hydroxydeoxyguanosine, hydroxyl free radical adduct of DNA in granulocytes exposed to the tumor promotor, tetradeconylphorbolacetate. Biochem. Biophys. Res. Commun. 137, 841-846
52. Floyd, R. A., West, M. S., Eneff, K. L., Hogsett, W. E., and Tingey, D. T. (1988) Hydroxyl free radical mediated formation of 8-hydroxyguanine in isolated DNA. Arch. Biochem. Biophys. 262, 266-272
53. Gupta, R. G. (1984) Nonrandom binding of the carcinogen N-hydroxy-2-aretylaminofluorene to repetitive sequences of rate liver DNA in vivo. Proc. Natl Acad. Sci. USA 81, 6943-6947
54. Shigenaga, M. K., Aboujaoude, E. N., Chen, Q., and Ames, B. N. (1994) [2] Assays of oxidative DNA damage biomarkers 8-oxo-2′-deoxyguanosine and 8-oxoguanine in nuclear DNA and biological fluids by high-performance liquid chromatography with electrochemical detection. Methods Enzymol. 234, 16-33
55. Shigenaga, M. K., Park, J. W., Cundy, K. C., Gimeno, C. J., and Ames, B. N. (1990) [54] In vivo oxidative DNA damage: measurement of 9-hydroxy-2′-deoxyguanosine in DNA and urine by high-performance liquid chromatography with electrochemical detection. Methods Enzymol. 186, 521-530
56. Liu, D. (1993) Generation and detection of hydroxyl radical in vivo in rat spinal cord by microdialysis administration of Fenton's reagents and microdialysis sampling. J. Biochem. Biophys. Methods 27, 281-293
57. Liu, D., Yang, R., Yan, X., and McAdoo, D. J. (1994) Hydroxyl radical generated in vivo kill neurons in spinal cord: Electrophysiological, histological, and neurochemical results. J. Neurochem. 62, 37-44
58. Liu, D., Yang, J., Li, L., and McAdoo, D. J. (1995) Paraquat - a superoxide generator - kills neurons in the rat spinal cord. Free Rad. Biol. Med, 18, 861-867
59. 2α rises in response to hydroxyl radical generated in vivo. Free Rad. Biol. Med. 18, 571-576
60. Liu, R., Althaus, J. S., Ellerbrock, 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, 763-770
61. Aguirre, T., Bosch, L. Van Den, Goetschalckx, K., Tilkin, R. N., Mathijs, G., Cassiman, J. J., and Robberecht, W. (1998) Increased sensitivity of fibroblasts from amyotrophic lateral sclerosis patients to oxidative stress. Ann. Neurol. 43, 452-457
62. Kaur, H., Whiteman, M., and Halliwell, B. (1997) Peroxynitritedependent aromatic hydroxylation and nitration of salicylate and phenylalanine. Is hydroxyl radical involved? Free Rad. Res. 26, 71-82
63. Halliwell, B., and Kaur, H. (1997) Hydroxylation of salicylate and phenylalanine as assays for hydroxyl radicals: a cautionary note visited for the third time. Free Rad. Res. 27, 239-244
64. Narayan, M., Berliner, L. J., Merola, A. J., Diaz, P. T., and Clanton, T. L. (1997) Biological reactions of peroxynitrite: evidence for an alternative pathway of salicylate hydroxylation. Free Rad. Res. 27, 63-72
65. Liu, D., Wen, J., and Liu, J. (1997) The cause of amyotrophic lateral sclerosis. J. Neurotrauma 14, 785
66. Pardo, C. A., Zuoshang, X., Borchelt, D. R., and Price, D. L. (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