ALS-linked Cu/Zn-SOD mutation increases vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis

Experimental Neurology

Volumn 160, Issue 1, 1999, Pages 28-39

  Kruman, Inna I ^a   Pedersen, Ward A ^a   Springer, Joe E ^a   Mattson, Mark P ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; AMPA RECEPTOR; COPPER ZINC SUPEROXIDE DISMUTASE; ESTRADIOL; EXCITOTOXIN; GLUTAMIC ACID; NITRIC OXIDE; OXYGEN RADICAL; PEROXYNITRITE; SCAVENGER;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL LOSS; CELL PROTECTION; COCULTURE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE MUTATION; GENE OVEREXPRESSION; LIPID PEROXIDATION; MOTONEURON; MOUSE; MUTANT; NERVE CELL CULTURE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL;

EID: 0032731637     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7190     Document Type: Article

References (63)

1. Beal M. F., Ferrante R. J., Browne S. E., Matthews R. T., Kowall N. W., Brown R. H. Jr. Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann. Neurol. 42:1997;644-654.
2. Beal M. F. Mitochondrial dysfunction in neurodegenerative diseases. Biochim. Biophys. Acta. 1366:1998;211-223.
3. Bensimon G., Lacomblez L., Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis: ALS/Riluzole Study Group. N. Engl. J. Med. 330:1994;585-591.
4. Bindokas V. P., Jordan J., Lee C. C., Miller R. J. Superoxide production in rat hippocampal neurons: Selective imaging with hydroethidine. J. Neurosci. 16:1996;1324-1336.
5. Carriedo S. G., Yin H. Z., Weiss J. H. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J. Neurosci. 16:1996;4069-4079.
6. Choi D. W. Calcium: Still center stage in hypoxic-ischemic neuronal death. Trends Neurosci. 18:1996;58-60.
7. Couratier P., Hugon J., Sindou P., Vallat J. M., Dumas M. Cell culture evidence for neuronal degeneration in amyotrophic lateral sclerosis being linked to glutamate AMPA/kainate receptors. Lancet. 341:1993;265-268.
8. Ferrante R. J., Shinobu L. A., Schulz J. B., Matthews R. T., Thomas C. E., Kowall N. W., Gurney M. E., Beal M. F. Increased 3-nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Ann. Neurol. 42:1997;326-334.
9. Ferrante R. J., Browne S. E., Shinobu L. A., Bowling A. C., Baik M. J., MacGarvey U., Kowall N. W., Brown R. H. Jr, Beal M. F. Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J. Neurochem. 69:1997;2064-2074.
10. Goodman Y., Mattson M. P. Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid β-peptide toxicity. J. Neurochem. 66:1996;869-872.
11. Goodman Y., Bruce A. J., Cheng B., Mattson M. P. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury and amyloid β-peptide toxicity in hippocampal neurons. J. Neurochem. 66:1996;1836-1844.
12. Greensmith L., Mentis G. Z., Vrbova G. Blockade of N-methyl-D-aspartate receptors by MK-801 (dizocilpine maleate) rescues motoneurones in developing rats. Dev. Brain Res. 81:1994;162-170.
13. 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. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science. 264:1994;1772-1775.
14. Gurney M. E., Cutting F. B., Zhai P., Andrus P. K., Hall E. D. Pathogenic mechanisms in familial amyotrophic lateral sclerosis due to mutation of Cu, Zn superoxide dismutase. Pathol. Biol. (Paris). 44:1996;51-56.
15. Gurney M. E., Cutting F. B., Zhai P., Doble A., Taylor C. P., Andrus P. K., Hall E. D. Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Ann. Neurol. 39:1996;147-157.
16. Hirano A., Donnenfeld H., Sasaki S., Nakano I. Fine structural observations of neurofilamentous changes in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 43:1984;461-470.
17. Hosler B. A., Brown R. H. Jr. Superoxide dismutase and oxygen radical neurotoxicity. Curr. Opin. Neurol. 9:1996;486-491.
18. Hoth M., Fanger C. M., Lewis R. S. Mitochondrial regulation of store operated calcium signaling in T lymphocytes. J. Cell Biol. 137:1997;633-648.
19. Ikonomidou C., Qin Y., Labruyere J., Olney J. W. Motor neuron degeneration induced by excitotoxin agonists has features in common with those seen in the SOD-1 transgenic mouse model of amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 55:1996;211-224.
20. Keller J. N., Pang Z., Geddes J. W., Begley J. G., Germeyer A., Waeg G., Mattson M. P. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: Role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 69:1997;273-284.
21. Keller J. N., Kindy M. S., Holtsberg F. W., St Clair D. K., Yen H.-C., Germeyer A., Steiner S. M., Bruce-Keller A. J., Hutchins J. B., Mattson M. P. Mitochondrial MnSOD prevents neural apoptosis and reduces ischemic brain injury: Suppression of peroxynitrite production, lipid peroxidation and mitochondrial dysfunction. J. Neurosci. 18:1998;687-697.
22. Kong J., Xu Z. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J. Neurosci. 18:1998;3241-3250.
23. Kruman I., Mattson M. P. Pivotal role for mitochondrial calcium uptake in neural cell apoptosis and necrosis. J. Neurochem. 72:1999;529-540.
24. Lafon-Cazal M., Pietri S., Culcasi M., Bockaert J. NMDA-dependent superoxide production and neurotoxicity. Nature. 364:1993;535-537.
25. Leist M., Nicotera P. Calcium and neuronal death. Rev. Physiol. Biochem. Pharmacol. 132:1998;79-125.
26. Mark R. J., Lovell M. A., Markesbery W. R., Uchida K., Mattson M. P. A role for 4-hydroxynonenal in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68:1997;255-264.
27. Martinou J. C., Le Van Thai A., Cassar G., Roubinet F., Weber M. J. Characterization of two factors enhancing choline acetyltransferase activity in cultures of purified rat motoneurons. J. Neurosci. 9:1989;3645-3656.
28. Mattson M. P., Rychlik B., Chu C., Christakos S. Evidence for calcium-reducing and excitoprotective roles for the calcium binding protein (calbindin-D28k) in cultured hippocampal neurons. Neuron. 6:1991;41-51.
29. Mattson M. P., Zhang Y., Bose S. Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp. Neurol. 121:1993;1-13.
30. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J. Neurochem. 65:1995;1740-1751.
31. Mattson M. P., Mark R. J. Excitotoxicity and excitoprotection in vitro. Adv. Neurol. 71:1996;1-37.
32. Mattson M. P., Goodman Y., Luo H., Fu W., Furukawa K. Activation of NF-κB protects hippocampal neurons against oxidative stress-induced apoptosis: Evidence for induction of Mn-SOD and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49:1997;681-697.
33. Mattson M. P. Modification of ion homeostasis by lipid peroxidation: Roles in neuronal degeneration and adaptive plasticity. Trends Neurosci. 21:1998;53-57.
34. McCord J. M., Fridovich I. Superoxide dismutase: The first twenty years (1968-1988). Free Rad. Biol. Med. 5:1988;363-369.
35. Moncada C., Lekieffre D., Arvin B., Meldrum B. Effect of NO synthase inhibition on NMDA- and ischaemia-induced hippocampal lesions. NeuroReport. 3:1992;530-532.
36. Pedersen W. A., Fu W., Keller J. N., Markesbery W. R., Appel S., Smith R. G., Kasarskis E., Mattson M. P. Protein modification by the lipid peroxidation product 4-hydroxynonenal in the spinal cords of ALS patients. Ann. Neurol. 44:1998;819-824.
37. 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., Snider W. D. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nature Genet. 13:1996;43-47.
38. Ripps M. E., Huntley G. W., Hof P. R., Morrison J. H., Gordon J. W. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA. 92:1995;689-693.
39. Ross S. M., Roy D. N., Spencer P. S. Beta-N-oxalylamino-L-alanine action on glutamate receptors. J. Neurochem. 53:1989;710-715.
40. Rothstein J. D., Tsai G., Kuncl R. W., Clawson L., Cornblath D. R., Drachman D. B., Pestronk A., Stauch B. L., Coyle J. T. Abnormal excitatory amino acid metabolism in amyotrophic lateral sclerosis. Ann. Neurol. 28:1990;18-25.
41. Rothstein J. D., Martin L. J., Kuncl R. W. Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N. Engl. J. Med. 326:1992;1464-1468.
42. Rothstein J. D., Jin L., Dykes-Hoberg M., Kuncl R. W. Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc. Natl. Acad. Sci. USA. 90:1993;6591-6595.
43. Rothstein J. D. Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin. Neurosci. 3:1995;348-359.
44. Rothstein J. D., Van Kammen M., Levey A. I., Martin L. J., Kuncl R. W. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann. Neurol. 38:1995;73-84.
45. Roy J., Minotti S., Dong L., Figlewicz D. A., Durham H. D. Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci. 18:1998;9673-9684.
46. Samarasinghe S., Virgo L., de Belleroche J. Distribution of the N-methyl-D-aspartate glutamate receptor subunit NR2A in control and amyotrophic lateral sclerosis spinal cord. Brain Res. 727:1996;233-237.
47. Sasaki S., Iwata M. Ultrastructural study of synapses in the anterior horn neurons of patients with amyotrophic lateral sclerosis. Neurosci. Lett. 204:1996;53-56.
48. 3H]MK-801 binding sites in the normal human spinal cord. Brain Res. 539:1991;164-168.
49. 3H]kainate. Brain Res. 655:1994;186-194.
50. Siklos L., Engelhardt J., Harati Y., Smith R. G., Joo F., Appel S. H. Ultrastructural evidence for altered calcium in motor nerve terminals in amyotropic lateral sclerosis. Ann. Neurol. 39:1996;203-216.
51. Siklos L., Engelhardt J. I., Alexianu M. E., Gurney M. E., Siddique T., Appel S. H. Intracellular calcium parallels motoneuron degeneration in SOD-1 mutant mice. J. Neuropathol. Exp. Neurol. 57:1998;571-587.
52. Smith R. G., Henry Y. K., Mattson M. P., Appel S. H. Presence of 4-hydroxynonenal in cerebrospinal fluid of patients with sporadic amyotrophic lateral sclerosis. Ann. Neurol. 44:1998;696-699.
53. Spencer P. S., Hugon J., Ludolph A., Nunn P. B., Ross S. M., Roy D. N., Schaumburg H. H. Discovery and partial characterization of primate motor-system toxins. Ciba Found. Symp. 126:1987;221-238.
54. Squadrito G. L., Pryor W. A. Oxidative chemistry of nitric oxide: The roles of superoxide, peroxynitrite, and carbon dioxide. Free Rad. Biol. Med. 25:1998;392-403.
55. Susin S. A., Zamzami N., Kroemer G. Mitochondria as regulators of apoptosis: Doubt no more. Biochim. Biophys. Acta. 1366:1998;151-165.
56. Temkin R., Lowe D., Jensen P., Hatt H., Smith D. O. Expression of glutamate receptor subunits in α-motoneurons. Mol. Brain Res. 52:1997;38-45.
57. White R. J., Reynolds I. J. Mitochondrial depolarization in glutamate-stimulated neurons: An early signal specific to excitotoxin exposure. J. Neurosci. 16:1996;5688-5697.
58. Wiedau-Pazos M., Goto J. J., Rabizadeh S., Gralla E. B., Roe J. A., Lee M. K., Valentine J. S., Bredesen D. E. Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science. 271:1996;515-518.
59. Williams T. L., Ince P. G., Oakley A. E., Shaw P. J. An immunocytochemical study of the distribution of AMPA selective glutamate receptor subunits in the normal human motor system. Neuroscience. 74:1996;185-198.
60. Wong P. C., Pardo C. A., Borchelt D. R., Lee M. K., Copeland N. G., Jenkins N. A., Sisodia S. S., Cleveland D. W., Price D. L. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron. 14:1995;1105-1116.
61. Yim H. S., Kang J. H., Chock P. B., Stadtman E. R., Yim M. B. A familial amyotrophic lateral sclerosis-associated A4V Cu,Zn-superoxide dismutase mutant has a lower Km for hydrogen peroxide: Correlation between clinical severity and the Km value. J. Biol. Chem. 272:1997;8861-8863.
62. Yoshida M., Akaike T., Wada Y., Sato K., Ikeda K., Ueda S., Maeda H. Therapeutic effects of imidazolineoxyl N-oxide against endotoxin shock through its direct nitric oxide-scavenging activity. Biochem. Biophys. Res. Commun. 202:1994;923-930.
63. Zhang Y., Tatsuno T., Carney J., Mattson M. P. Basic FGF, NGF, and IGFs protect hippocampal neurons against iron-induced degeneration. J. Cereb. Blood Flow Metab. 13:1993;378-388.