Increased mitochondrial superoxide generation in neurons from trisomy 16 mice: A model of Down's syndrome

Free Radical Biology and Medicine

Volumn 28, Issue 2, 2000, Pages 235-250

  Schuchmann, Sebastian ^a   Heinemann, Uwe ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Alzheimer's disease; Down's syndrome; Free radicals; Hippocampal culture; NAD(P)H autofluorescence; Reactive oxygen species; Superoxide anion; Trisomy 16

Indexed keywords

ANTIMYCIN A1; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUPEROXIDE; UBIQUINONE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOFLUORESCENCE; AUTOOXIDATION; CONTROLLED STUDY; DIPLOIDY; DOWN SYNDROME; EMBRYO; ENERGY METABOLISM; FETUS; HIPPOCAMPUS; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NERVE DEGENERATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; TRISOMY;

ANIMALS; ANTIMYCIN A; CELL DEATH; CELLS, CULTURED; CHROMOSOME MAPPING; CYANIDES; DIPLOIDY; DISEASE MODELS, ANIMAL; DOWN SYNDROME; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; EMBRYONIC AND FETAL DEVELOPMENT; HIPPOCAMPUS; HUMANS; MICE; MICE, MUTANT STRAINS; MITOCHONDRIA; NADH, NADPH OXIDOREDUCTASES; NEURONS; REACTIVE OXYGEN SPECIES; ROTENONE; SUPEROXIDES; TRISOMY;

EID: 0033967558     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(99)00226-9     Document Type: Article

References (65)

1. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:1979;527-605.
2. Coyle J.T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 262:1993;689-695.
3. Schreck R., Rieber P., Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J. 10:1991;2247-2258.
4. Baeuerle P.A., Henkel T. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:1994;141-179.
5. Richter C., Gogvadze V., Laffranchi R., Schlapbach R., Schweizer M., Suter M., Walter P., Yaffee M. Oxidants in mitochondria from physiology to diseases . Biochim. Biophys. Acta. 1271:1995;67-74.
6. Slater A.F.G., Nobel C.S.I., Orrenius S. The role of intracellular oxidats in apoptosis. Biochim. Biophys. Acta. 1271:1995;59-62.
7. Sohal R.S., Weindruch R. Oxidative stress, caloric restriction, and aging. Science. 273:1996;59-63.
8. Harman D. The aging process. Proc. Natl. Acad. Sci. USA. 78:1981;7124-7128.
9. Lafon-Cazal M., Pietri S., Culcasi M., Bockaert J. NMDA-dependent superoxide production and neurotoxicity. Nature. 364:1993;535-537.
10. Behl C., Davis J.B., Lesley R., Schubert D. Hydrogen peroxide mediates amyloid β protein toxicity. Cell. 77:1994;817-827.
11. Ames B.N., Shigenaga M.K., Hagen T.M. Mitochondrial decay in aging. Biochim. Biophys. Acta. 1271:1995;165-170.
12. Busciglio J., Yankner B.A. Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature. 378:1995;776-779.
13. Mattson M.P. Free radicals and disruption of neuronal ion homeostasis in AD a role for amyloid β-peptide? Neurobiol. Aging. 16:1995;679-682.
14. Poyton R.O., McEwen J.E. Crosstalk between nuclear and mitochondrial genomes. Annu. Rev. Biochem. 65:1996;563-607.
15. Schinder A.F., Olson E.C., Spitzer N.C., Montal M. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci. 16:1996;6125-6133.
16. Zamzami N., Susin S.A., Marchetti P., Hirsch T., Gómez-Monterrey I., Castedo M., Kroemer G. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1996;1533-1544.
17. Zorov D.B. Mitochondrial damage as a source of diseases and aging a strategy of how to fight these . Biochim. Biophys. Acta. 1275:1996;10-15.
18. Zamzami N., Marchetti P., Castedo M., Zanin C., Vayssière J.-L., Petit P.X., Kroemer G. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1995;1661-1672.
19. 2+ signaling and mitochondrial deficiencies in hippocampal neurons of trisomy 16 mice a model of Down's syndrome . J. Neurosci. 18:1998;7216-7231.
20. Richards S.J. The neuropathology of Alzheimer's disease investigated by transplantation of mouse trisomy 16 hippocampal tissues. Trends Neurosci. 14:1991;334-338.
21. Holtzman D.M., Bayney R.M., Li Y., Khosrovi H., Berger C.N., Epstein C.J., Mobley W.C. Dysregulation of gene expression in mouse trisomy 16, an animal model of Down's syndrome. EMBO J. 11:1992;619-627.
22. Epstein C.J. The neurobiology of Down's syndrome. 1986;Raven Press, New York.
23. 2+ homeostasis, cell death, proliferation, and differentiation . Chem. Biol. Interact. 77:1991;1-23.
24. 2+ homeostase in Alzheimer's disease. Trends Neurosci. 16(10):409-414; 1993.
25. Gunter T.E., Gunter K.K., Sheu S.-S., Gavin C.E. Mitochondrial calcium transport physiological and pathological relevance . Am. J. Physiol. 267:1994;C313-C339.
26. Richards S.J., Waters J.J., Beyreuther K., Masters C.L., Wischik C.M., Sparkman D.R., White C.L., Abraham C.R., Dunnett S.B. Transplants of mouse trisomy 16 hippocampus provide a model of Alzheimer's disease neuropathology. EMBO J. 10:1991;297-303.
27. Hensley K., Carney J.M., Mattson M.P., Aksenova M., Harris M., Wu J.F., Floyd R.A., Butterfield D.A. A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide relevance to Alzheimer's disease . Proc. Natl. Acad. Sci. USA. 91:1994;3270-3274.
28. Mattson M.P., Goodman Y. Different amyloidogenic peptides share a similar mechanism of neurotoxicity involving reactive species and calcium. Brain Res. 676:1995;219-224.
29. Duke J.B. The biology of oxygen radicals. Science. 201:1978;875-880.
30. Peled-Kamar M., Lotem J., Okon E., Sachs L., Groner Y. 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. 14:1995;4985-4993.
31. Bambrick L.L., Yarowsky P.J., Krueger B.K. Glutamate as a hippocampal neuron survival factor an inherited defect in the trisomy 16 mouse . Proc. Natl. Acad. Sci. USA. 92:1995;9692-9696.
32. Stabel-Burow J., Kleu A., Schuchmann S., Heinemann U. Glutathione levels and nerve cell loss in hippocampal cultures from trisomy 16 mouse - a model of Down's syndrome. Brain Res. 765:1997;313-318.
33. Gropp A., Kolbus U., Giers D. Systematic approach to the study of trisomy in the mouse. II. Cytogenet. Cell Genet. 14:1975;42-62.
34. Banker G.A., Cowan W.M. Rat hippocampal neurons in dispersed cell culture. Brain Res. 126:1977;397-425.
35. Lane N.J., Balbo A., Rapoport S.I. A fine structural study of hippocampus and dorsal root ganglion in mouse trisomy 16, a model of Down's syndrome. Cell Biol. Int. 20:1996;673-680.
36. Bindokas V.P., Jordán J., Lee C.C., Miller R.J. Superoxide production in rat hippocampal neurons selective imaging with hydroethidine . J. Neurosci. 16:1996;1324-1336.
37. Oyama Y., Hayashi A., Ueha T., Maekawa K. Characterization of 2′,7′-dichlorofluorescin fluorescence in dissociated mammalian brain neurons estimation on intracellular content of hydrogen peroxide . Brain Res. 635:1994;113-117.
38. Aubin J.E. Autofluorescence of viable cultured mammalian cells. J. Histochem. Cytochem. 27:1979;36-43.
39. 2+-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem. J. 283:1992;41-50.
40. Benson R.C., Meyer R.A., Zaruba M.E., McKhann G.M. Cellular autofluorescence - is it due to flavins? J. Histochem. Cytochem. 27:1979;44-48.
41. Lai J.C.K., Clark J.B. Preparation of synaptic and nonsynaptic mitochondria from mammalian brain. Methods Enzymol. 55:1979;51-60.
42. Sherratt H.S.A., Watmough N.J., Johnson M.A., Turnbull D.M. Methods for the study of normal and abnormal skeletal muscle mitochondria. Methods Biochem. Anal. 33:1988;243-335.
43. Birch-Machin M.A., Shepherd I.M., Watmough N.J., Sherratt H.S.A., Bartlett K., Darley-Usmar V.M., Milligan D.W.A., Welch R.J., Aynsley-Green A., Turnbull D.M. Fatal lactic acidosis in infancy with a defect of complex III of the respiratory chain. Pediatr. Res. 25:1989;553-559.
44. Turrens J.F., Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem. J. 191:1980;421-427.
45. Zhang Y., Marciallat O., Giulivi C., Ernster L., Davies K.J.A. The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265:1990;16330-16336.
46. Cardoso S.M., Pereira C., Oliveira C.R. Mitochondrial function is differentially affected upon oxidative stress. Free Radic. Biol. Med. 26:1999;3-13.
47. Reynolds I.J., Hastings T.G. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15:1995;3318-3327.
48. Chance B. Pyridine nucleotide as an indicator of oxygen requirements for energy-linked functions of mitochondria. Circ. Res. 38:(Suppl. 1):1976;31-38.
49. Scanlon J.M., Reynolds I.J. Effects of oxidants and glutamate receptor activation on mitochondrial membrane potential in rat forebrain neurons. J. Neurochem. 71:1998;2392-2400.
50. Ames B.N., Shigenaga M.K., Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA. 90:1993;7915-7922.
51. Friedlich A.L., Butcher L.L. Involvement of free oxygen radicals in β-amyloidosis an hypothesis . Neurobiol. Aging. 15:1994;443-455.
52. Kelner M.J., Bagnell R., Montoya M., Estes L., Uglik S.F., Cerutti P. Transfection with human copper-zinc superoxide dismutase induced bidirectional alterations in other antioxidant enzymes, proteins, growth factor response, and paraquat resistance. Free Radic. Biol. Med. 18:1995;497-506.
53. Yim M.B., Chock P.B., Stadtman E.R. Enzyme function of copper, zinc superoxide dismutase as a free radical generator. J. Biol. Chem. 268:1993;4099-4105.
54. Sinet P.M. Metabolism of oxygen derivatives in Down's syndrome. Ann. N. Y. Acad. Sci. 396:1982;83-94.
55. Ceballos-Picot I., Nicole A., Briand P., Grimber G., Delacourte A., Defossez A., Javoy-Agid F., Lafon M., Blouin J.L., Sinet P.M. Neuronal-specific expression of human copper-zinc superoxide dismutase gene in transgenic mice animal model of gene dosage effects in Down's syndrome . Brain Res. 552:1991;198-214.
56. Dugan L.L., Sensi S.L., Canzoniero L.M.T., Handran S.D., Rothman S.M., Lin T.-S., Goldberg M.P., Choi D.W. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15:1995;6377-6388.
57. Bandy B., Davison A.J. Mitochondrial mutations may increase oxidative stress implications for carcinogenesis and aging? Free Radic. Biol. Med. 8:1990;523-539.
58. Malis C.D., Bonventre J.V. Mechanism of calcium potentiation of oxygen free radical injury to renal mitochondria. J. Biol. Chem. 261:1986;14201-14208.
59. + implications for neurodegeneration . J. Neurochem. 63:1994;584-591.
60. Cadenas E., Boveris A. Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria. Biochem. J. 188:1980;31-37.
61. Ernster L., Dallner G. Biochemical, physiological and medical aspects of ubiquinone function. Biochim. Biophys. Acta. 1271:1995;195-204.
62. Bindokas V.P., Chong C.L., Colmers W.F., Miller R.J. Changes in mitochondrial function resulting from synaptic activity in the rat hippocampal slice. J. Neurosci. 18:1998;4570-4587.
63. Duchen M.R., Smith P.A., Ashcroft F.M. Substrate-dependent changes in mitochondrial function, intracellular free calcium concentration and membrane channels in pancreatic β-cells. Biochem. J. 294:1993;35-42.
64. 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.
65. Richter C., Park J.-W., Ames B.N. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc. Natl. Acad. Sci. USA. 85:1988;6465-6467.