Variation in the biochemical/biophysical properties of mutant superoxide dismutase 1 enzymes and the rate of disease progression in familial amyotrophic lateral sclerosis kindreds

Human Molecular Genetics

Volumn 8, Issue 8, 1999, Pages 1451-1460

  Ratovitski, Tamara ^a   Corson, Laura B ^b   Strain, Jeffrey ^c   Wong, Philip ^a   Cleveland, Don W ^b   Culotta, Valeria C ^c   Borchelt, David R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; COPPER; HISTIDINE; MUTANT PROTEIN; SUPEROXIDE DISMUTASE; VALINE;

AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; GENE MUTATION; LIFE EXPECTANCY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SOLUBILITY;

AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CENTRIFUGATION; COPPER; COS CELLS; DISEASE PROGRESSION; ENDOPEPTIDASE K; FAMILY HEALTH; GLYCINE; HISTIDINE; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; PROTEIN BINDING; SOLUBILITY; SUPEROXIDE DISMUTASE; TIME FACTORS; TUMOR CELLS, CULTURED; VARIATION (GENETICS);

ANIMALIA;

EID: 0032815965     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/8.8.1451     Document Type: Article

References (62)

1. Price, D.L., Martin, L.J., Clatterbuck, R.E., Koliatsos, V.E., Sisodia, S.S., Walker, L.C. and Cork, L.C. (1992) Neuronal degeneration in human diseases and animal models. J. Neurobiol., 23, 1277-1294.
2. Rowland, L.P. (1994) In Calne, D.B. (ed.), Neurodegenerative Diseases. W.B. Saunders, Philadelphia, PA, pp. 507-521.
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. 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, 362, 59-62.
5. Fridovich, I. (1986) Superoxide dismutases. Adv. Enzymol. Relat. Areas Mol. Biol., 58, 61-97.
6. Cizewski Culotta, V., Joh, H.-D., Lin, S.-J., Hudak Slekar, K. and Strain, J. (1995) A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. J. Biol. Chem., 270, 29991-29997.
7. Borchelt, D.R., Lee, M.K., Slunt, H.H., Guarnieri, M., Xu, Z.-S., Wong, P.C., Brown, R.H.Jr, Price, D.L., Sisodia, S.S. and Cleveland, D.W. (1994) Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc. Natl Acad. Sci. USA, 91, 8292-8296.
8. Rabizadeh, S., Butler Gralla, E., Borchelt, D.R., Gwinn, R., Selverstone Valentine, J., Sisodia, S., Wong, P., Lee, M., Hahn, H. and Bredesen, D.E. (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.
9. Borchelt, D.R., Guarnieri, M., Wong, P.C., Lee, M.K., Slunt, H.S., Xu, Z.-S., Sisodia, S.S., Price, D.L. and Cleveland, D.W. (1995) Superoxide dismutase 1 subunits with mutations linked to familial amyotrophic lateral sclerosis do not affect wild-type subunit function. J. Biol. Chem., 270, 3234-3238.
10. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., 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.
11. Wong, P.C., Pardo, C.A., Borchelt, D.R., Lee, M.K., Copeland, N.G., Jenkins, N.A., Sisodia, S.S., Cleveland, D.W. and Price, D.L. (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.
12. Bruijn, L.I., Becher, M.W., Lee, M.K., Anderson, K.L., Jenkins, N.A., Copeland, N.G., Sisodia, S.S., Rothstein, J.D., Borchelt, D.R., Price, D.L. and Cleveland, D.W. (1997) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron, 18, 327-338.
13. Corson, L.B., Culotta, V.C. and Cleveland, D.W. (1998) Chaperone-facilitated copper binding is a property common to several classes of familial amyotrophic lateral sclerosis-linked superoxide dismutase mutants. Proc. Natl Acad. Sci. USA, 95, 6361-6366.
14. Reaume, A.G., Elliott, J.L., Hoffman, E.K., Kowall, N.W., Ferrante, R.J., Siwek, D.F., Wilcox, H.M., Flood, D.G., Beal, M.F., Brown, R.H.Jr, Scott, R.W. and Snider, W.D. (1996) Motor neurons in Cu,Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nature Genet., 13, 43-47.
15. Ripps, M.E., Huntley, G.W., Hof, P.R., Morrison, J.H. and Gordon, J.W. (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.
16. Cleveland, D.W., Laing, N., Hurse, P.V. and Brown, R.H.Jr (1995) Toxic mutants in Charcot's sclerosis. Nature, 378, 342-343.
17. Radunovic, A. and Leigh, P.N. (1996) Cu/Zn superoxide dismutase gene mutations in amyotrophic lateral sclerosis: correlation between genotype and clinical features. J. Neurol. Neurosurg. Psychiatr., 61, 565-572.
18. Juneja, T., Pericak-Vance, M.A., Laing, N.G., Dave, S. and Siddique, T. (1997) Prognosis in familial amyotrophic lateral sclerosis: progression and survival in patients with glu100gly and ala4val mutations in Cu,Zn superoxide dismutase. Neurology, 48, 55-57.
19. Parge, H.E., Hallewell, R.A. and Tainer, J.A. (1992) Atomic structures of wild-type and thermostable mutant recombinant human Cu,Zn superoxide dismutase. Proc. Natl Acad. Sci. USA, 89, 6109-6113.
20. 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.
21. Enayat, Z.E., Orrell, R.W., Claus, A., Ludolph, A., Bachus, R., Brockmüller, J., Ray-Chaudhuri, K., Radunovic, A., Shaw, C., Wilkinson, J., King, A., Swash, M., Leigh, P.N., 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.
22. Chang, E.C., Crawford, B.F., Hong, Z., Bilinski, T. and Kosman, D.J. (1991) Genetic and biochemical characterization of Cu,Zn superoxide dismutase mutants in Saccharomyces cerevisiae. J. Biol. Chem., 266, 4417-4424.
23. 2-dependent methionine auxotrophy in Cu,Zn superoxide dismutase-deficient mutants of Saccharomyces cerevisiae. J. Bacteriol., 172, 1840-1845.
24. Liochev, S.I., Chen, L.L., Hallewell, R.A. and Fridovich, I. (1997) Superoxide-dependent peroxidase activity of H48Q: a superoxide dismutase variant associated with familial amyotrophic lateral sclerosis. Arch. Biochem. Biophys., 346, 263-268.
25. Pramatarova, A., Goto, J., Nanba, E., Nakashima, K., Takahashi, K., Takagi, A., Kanazawa, I., Figlewicz, D.A. and Rouleau, G.A. (1994) A , two basepair deletion in the SOD 1 gene causes familial amyotrophic lateral sclerosis. Hum. Mol. Genet., 3, 2061-2062.
26. Borchelt, D.R., Wong, P.C., Becher, M.W., Pardo, C.A., Lee, M.K., Xu, Z.-S., Thinakaran, G., Jenkins, N.A., Copeland, N.G., Sisodia, S.S., Cleveland, D.W., Price, D.L. and Hoffman, P.N. (1998) Axonal transport of mutant superoxide dismutase 1 and focal axonal abnormalities in the proximal axons of transgenic mice. Neurobiol. Dis., 5, 27-35.
27. 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.
28. Borchelt, D.R., Wong, P.C., Becher, M.W., Bruijn, L.I., Cleveland, D.W., Copeland, N.G., Culotta, V.C., Jenkins, N.A., Lee, M.K., Pardo, C.A., Price, D.L., Sisodia, S.S. and Xu, Z.-S. (1997) In Connor, J.R. (ed.), Metals and Oxidative Damage in Neurological Disorders. Plenum Press, New York, NY, pp. 295-314.
29. Shibata, N., Hirano, A., Kobayashi, M., Siddique, T., Deng, H.-X., Hung, W.-Y., Kato, T. and Asayama, K. (1996) Intense superoxide dismutase-1 immunoreactivity in intracytoplasmic hyaline inclusions of familial amyotrophic lateral sclerosis with posterior column involvement. J. Neuropathol. Exp. Neurol., 55, 481-490.
30. McKinley, M.P., Bolton, D.C. and Prusiner, S.B. (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell, 35, 57-62.
31. McKinley, M.P., Meyer, R.K., Kenaga, L., Rahbar. F., Cotter, R., Serban, A. and Prusiner, S.B. (1991) Scrapie prion rod formation in vitro requires both detergent extraction and limited proteolysis. J. Virol., 65, 1340-1351.
32. Glenner, G.G., Terry, W.D. and Isersky, C. (1973) Amyloidosis: its nature and pathogenesis. Semin. Hematol., 10, 65-86.
33. Glenner, G.G. and Wong, C.W. (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun., 120, 885-890.
34. Masters, C.L., Simms, G., Weinman, N.A., Multhaup, G., McDonald, B.L. and Beyreuther, K. (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl Acad. Sci. USA. 82, 4245-4249.
35. Dal Canto, M.C. and Gurney, M.E. (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.
36. Dal Canto, M.C, Mourelatos, Z., Gonatas, N.K., Chiu, A. and Gurney, M.E. (1996) In Nakano, I. and Hirano, A. (eds), Amyotrophic Lateral Sclerosis. Progress and Perspectives in Basic Research and Clinical Application. Elsevier, Amsterdam, pp. 331-338.
37. Dal Canto, M.C. and Gurney, M.E. (1997) A low expressor line of transgenic mice carrying a mutant human Cu,Zn superoxide dismutase (SOD1) gene develops pathological changes that most closely resemble those in human amyotrophic lateral sclerosis. Acta Neuropathol, 93, 537-550.
38. Andersen, P.M., Nilsson, P., Ala-Hurula, V., Keränen, M.-L., Tarvainen, I., Haltia, T., Nilsson, L., Binzer, M., Forsgren, L. and Marklund, S.L. (1995) Amyotrophic lateral sclerosis associated with homozygosity for an Asp90Ala mutation in CuZn-superoxide dismutase. Nature Genet., 10, 61-66.
39. Robberecht, W., Aguirre, T., Van Den Bosch, L., Tilkin, P., Cassiman, J.J. and Matthijs, G. (1996) D90A heterozygosity in the SOD1 gene is associated with familial and apparently sporadic amyotrophic lateral sclerosis. Neurology, 47, 1336-1339.
40. Al-Chalabi, A., Andersen, P.M., Chioza, B., Shaw, C., Sham, P.C., Robberecht, W., Matthijs, G., Camu, W., Marklund, S.L., Forsgren, L., Rouleau, G., Laing, N.G., Hurse, P.V., Siddique, T., Leigh, P.N. and Powell, J.F. (1998) Recessive amyotrophic lateral sclerosis families with the D90A SOD1 mutation share a common founder: evidence for a 1 inked protective factor. Hum. Mol. Genet., 7, 2045-2050.
41. 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, 515-518.
42. m for hydrogen peroxide. Proc. Natl Acad. Sci. USA, 93, 5709-5714.
43. Beckman, J.S., Ischiropoulos, H., Zhu, L., van der Woerd, M., Smith, C., Chen, J., Harrison, J., Martin, J.C. and Tsai, M. (1992) Kinetics of superoxide dismutase-and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys., 298, 438-445.
44. Beckman, J.S., Carson, M., Smith, C.D. and Koppenol, W.H. (1993) ALS, SOD and peroxynitrite. Nature, 364, 584.
45. 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, 1936-1944.
46. Crow, J.P., Ye, Y.Z., Strong, M., Kirk, M., Barnes, S. and Beckman, J.S. (1997) Superoxide dismutase catalyzes nitration of tyrosines by peroxynitrite in the rod and head domains of neurofilament-L. J. Neurochem., 69, 1945-1953.
47. Carri, M.T., Battistoni. A., Polizio, F., Desideri, A. and Rotilio, G. (1994) Impaired copper binding by the H46R mutant of human Cu,Zn superoxide dismutase, involved in amyotrophic lateral sclerosis. FEBS Lett., 356, 314-316.
48. Culotta, V.C., Klomp, L.W.J., Strain, J., Casareno, R.L.B., Krems, B. and Gitlin, G.D. (1997) The copper chaperone for superoxide dismutase. J. Biol. Chem., 272, 23469-23472.
49. Keele, B.B.Jr, McCord, J.M. and Fridovich, I. (1970) Superoxide dismutase from Escherichia coli B. A new manganese-containing enzyme. J. Biol. Chem., 245, 6176-6181.
50. Yost, F.J.Jr and Fridovich, I. (1973) An iron-containing superoxide dismutase from Escherichia coli. J. Biol. Chem., 248, 4905-4908.
51. Lyons, T.J., Liu, H., Goto, J.J., Nersissian, A., Roe, J.A., Graden, J.A., Café, C., Ellerby, L.M., Bredesen, D.E., Gralla, E.B. and Valentine, J.S. (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, 12240-12244.
52. Brown, R.H.Jr (1995) Amyotrophic lateral sclerosis: recent insights from genetics and transgenic mice. Cell, 80, 687-692.
53. Durham, H.D., Roy, J., Dong, L. and Figlewicz, D.A. (1997) Aggregation of mutation Cu/Zn superoxide dismutase proteins in a culture model of ALS. J. Neuropathol. Exp. Neurol., 56, 523-530.
54. 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, 693-699.
55. Mizushima, S. and Nagata, S. (1990) pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res., 18, 5322.
56. Becker, D.M. and Guarente, L. (1991) High-efficiency transformation of yeast by electrophoration. Methods Enzymol., 194, 187.
57. Pardo, C.A., Xu, Z., Borchelt, D.R., Price, D.L., Sisodia, S.S. and Cleveland, D.W. (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.
58. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol., 7, 2745-2752.
59. Beauchamp, C. and Fridovich, I. (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem., 44, 276-287.
60. Cudkowicz, M.E., McKenna-Yasek, D., Sapp, P.E., Chin, W., Geller, B., Hayden, D.L., Schoenfeld, D.A., Hosler, B.A., Horvitz, H.R. and Brown, R.H. (1997) Epidemiology of mutations in superoxide dismutase in amyotrophic lateral sclerosis. Ann. Neurol., 41, 210-221.
61. Laing, N.G. and Siddique, T. (1996) Cu/Zn superoxide dismutase gene mutations in amyotrophic lateral sclerosis: correlation between genotype and clinical features. J. Neurol. Neurosurg. Psychiatr., 63, 815-815.
62. McCord, J.M. and Fridovich, I. (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem., 244, 6049-6055.