Increased vulnerability of hippocampal neurons from presenilin-1 mutant knock-in mice to amyloid β-peptide toxicity: Central roles of superoxide production and caspase activation

Journal of Neurochemistry

Volumn 72, Issue 3, 1999, Pages 1019-1029

  Guo, Qing ^a   Sebastian, Lois ^a   Sopher, Bryce L ^b   Miller, Miles W ^b   Ware, Carol B ^b   Martin, George M ^b   Mattson, Mark P ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer's disease; Mitochondrial transmembrane potential; Peroxynitrite; Uric acid

Indexed keywords

AMYLOID BETA PROTEIN; ANTIOXIDANT; CASPASE; PEROXYNITRITE; PRESENILIN 1; SUPEROXIDE; URIC ACID;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL MODEL; ARTICLE; ENZYME ACTIVATION; GENE MUTATION; HIPPOCAMPUS; KNOCKOUT MOUSE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MOUSE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; CASPASES; CELL SURVIVAL; CELLS, CULTURED; ENZYME ACTIVATION; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MUTATION; NEURONS; PRESENILIN-1; REACTIVE OXYGEN SPECIES; SUPEROXIDES;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0033009194     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0721019.x     Document Type: Article

References (80)

1. Ancolio K., Marambaud P., Dauch P., and Checler F. (1997) α-Secretase-derived product of β-amyloid precursor protein is decreased by presenilin 1 mutations linked to familial Alzheimer's disease. J. Neurochem. 69, 2494-2499.
2. Beckman J. S. and Crow J. P. (1993) Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochem. Soc. Trans. 21, 330-334.
3. Behl C., Davis J., Cole G. M., and Schubert D. (1992) Vitamin E protects nerve cells from amyloid beta protein toxicity. Biochem. Biophys. Res. Commun. 186, 944-950.
4. Behl C., Davis J. B., Lesley R., and Schubert D. (1994) Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77, 817-827.
5. Benzi G. and Moretti A. (1997) Contributions of mitochondrial alterations to brain aging. Adv. Cell Aging Gerontol. 2, 129-160.
6. Bindokas V. P., Jordan J., Lee C. C., and Miller R. J. (1996) Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci. 16, 1324-1336.
7. Borchelt D. R., Thinakaran G., Eckman C. B., Lee M. K., Davenport F., Ratovitsky T., Prada C.-M., Kim G., Seekins S., Yager D., Slunt H. H., Wang R., Seeger M., Levey A. I., Gandy S. E., Copeland N. G., Jenkins N. A., Price D. L., Younkin S. G., and Sisodia S. S. (1996) Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ1-42/1-40 ratio in vitro and in vivo. Neuron 17, 1005-1013.
8. Brockhaus M., Grunberg J., Rohrig S., Loetscher H., Wittenburg N., Baumeister R., Jacobsen H., and Haass C. (1998) Caspase-mediated cleavage is not required for the activity of presenilins in amyloidogenesis and NOTCH signaling. Neuroreport 9, 1481-1486.
9. Bruce A. J., Bose S., Fu W., Butt C. M., Mirault E. M., Taniguchi N., and Mattson M. P. (1997) Amyloid β-peptide alters the profile of antioxidant enzymes in hippocampal cultures in a manner similar to that observed in Alzheimer's disease. Pathogenesis 1, 15-30.
10. Busciglio J. and Yankner B. A. (1995) Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 378, 776-779.
11. Busciglio J., Lorenzo A., Yeh J., and Yankner B. A. (1995) β-Amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14, 879-888.
12. Butterfield D. A., Hensley K., Harris M., Mattson M. P., and Carney J. (1994) β-Amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer's disease. Biochem. Biophys. Res. Commun. 200, 710-715.
13. Buxbaum J. D., Ruefli A. A., Parker C. A., Cypess A. M., and Greengard P. (1994) Calcium regulates processing of the Alzheimer amyloid protein precursor in a protein kinase C-independent manner. Proc. Natl. Acad. Sci. USA 91, 4489-4493.
14. Davis J. A., Naruse S., Chen H., Eckman C., Younkin S., Price D. L., Borchelt D. R., Sisodia S. S., and Wong P. C. (1998) An Alzheimer's disease-linked PS1 variant rescues the developmental abnormalities of PS1-deficient embryos. Neuron 20, 603-609.
15. Doan A., Thinakaran G., Borchelt D. R., Slunt H. H., Ratovistsky T., Podlisny M., Selkoe D. J., Seeger M., Gandy S. E., Price D. L., and Sisodia S. S. (1996) Protein topology of presenilin 1. Neuron 17, 1023-1030.
16. Duff K., Eckman C., Zehr C., Yu X., Prada C.-M., Perez-Tur J., Hutton M., Buee L., Harigaya Y., Yager D., Morgan D., Gordon M. N., Holcomb L., Refolo L., Zenk B., Hardy J., and Younkin S. (1996) Increased amyloid-β42(43) in brains of mice expressing mutant presenilin 1. Nature 383, 710-713.
17. Furukawa K., Sopher B. L., Rydel R. E., Begley J. G., Martin G. M., Fox M., and Mattson M. P. (1996) Increased activity-regulating and neuroprotective efficacy of α-secretase-derived secreted amyloid precursor protein conferred by a C-terminal heparin-binding domain. J. Neurochem. 67, 1882-1896.
18. Furukawa K., Fu W., Witke W., Kwiatkowski D. J., and Mattson M. P. (1997) The actin-severing protein gelsolin modulates calcium channel activity and vulnerability to excitotoxicity in hippocampal neurons. J. Neurosci. 17, 8178-8186.
19. Gabuzda D., Busciglio J., Chen L., Matsudaira P., and Yankner B. A. (1994) Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative. J. Biol. Chem. 269, 13623-13628.
20. Gasparini L., Racchi M., Benussi L., Curti D., Binetti G., Bianchetti A., Trabucchi M., and Govoni S. (1997) Effect of energy shortage and oxidative stress on amyloid precursor protein metabolism in COS cells. Neurosci. Lett. 231, 113-117.
21. Geula C., Wu C. K., Saroff D., Lorenzo A., Yuan M., and Yankner B. A. (1998) Aging renders the brain vulnerable to amyloid β-protein neurotoxicity. Nat. Med. 4, 827-831.
22. Good P. F., Werner P., Hsu A., Olanow C. W., and Perl D. P. (1996) Evidence of neuronal oxidative damage in Alzheimer's disease. Am. J. Pathol. 149, 21-28.
23. Goodman Y. and Mattson M. P. (1994) Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peptide-induced oxidative injury. Exp. Neurol. 128, 1-12.
24. Goodman Y. and Mattson M. P. (1996) Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid β-peptide toxicity. J. Neurochem. 66, 869-872.
25. Goodman Y., Bruce A. J., Cheng B., and Mattson M. P. (1996) Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury and amyloid β-peptide toxicity in hippocampal neurons. J. Neurochem. 66, 1836-1844.
26. Guo Q., Furukawa K., Sopher B. L., Pham D. G., Xie J., Robinson N., Martin G. M., and Mattson M. P. (1996) Alzheimer's PS-1 mutation perturbs calcium homeostasis and sensitizes PC12 cells to death induced by amyloid β-peptide. Neuroreport 8, 379-383.
27. Guo Q., Sopher B. L., Pham D. G., Furukawa K., Robinson N., Martin G. M., and Mattson M. P. (1997) Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid β-peptide: involvement of calcium and oxyradicals. J. Neurosci. 17, 4212-4222.
28. Guo Q., Christakos S., Robinson N., and Mattson M. P. (1998a) Calbindin blocks the pro-apoptotic actions of mutant presenilin-1: reduced oxidative stress and preserved mitochondrial function. Proc. Natl. Acad. Sci. USA 95, 3227-3232.
29. Guo Q., Fu W., Xie J., Luo H., Sells S. F., Geddes J. W., Bondada V., Rangnekar V. M., and Mattson M. P. (1998b) Par-4 is a mediator of neuronal degeneration associated with the pathogenesis of Alzheimer disease. Nat. Med. 4, 957-962.
30. Guo Q., Robinson N., and Mattson M. P. (1998c) Secreted APPα counteracts the pro-apoptotic action of mutant presenilin-1 by activation of NF-ΚB and stabilization of calcium homeostasis. J. Biol. Chem. 273, 12341-12351.
31. Guo Q., Fu W., Sopher B. L., Miller M. W., Ware C. B., Martin G. M., and Mattson M. P. (1999) Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knockin mice. Nat. Med. (in press).
32. Hardy J. (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci. 20, 154-159.
33. Hooper D. C., Spitsin S., Kean R. B., Champion J. M., Dickson G. M., Chaudhry I., and Koprowski H. (1998) Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proc. Natl. Acad. Sci. USA 95, 675-680.
34. Hu J. and el-Fakahany E. E. (1993) β-Amyloid 25-35 activates nitric oxide synthase in a neuronal clone. Neuroreport 4, 760-762.
35. Janicki S. and Monteiro M. J. (1997) Increased apoptosis arising from increased expression of the Alzheimer's disease-associated presenilin-2 mutation (N141I). J. Cell Biol. 139, 485-495.
36. Keller J. N., Pang Z., Geddes J. W., Begley J. G., Germeyer A., Waeg G., and Mattson M. P. (1997) 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, 273-284.
37. 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., and Mattson M. P. (1998) Mitochondrial MnSOD prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation and mitochondrial dysfunction. J. Neurosci. 18, 687-697.
38. Kim T. W. and Tanzi R. E. (1997) Presenilins and Alzheimer's disease. Curr. Opin. Neurobiol. 7, 683-688.
39. Kim T.-W., Pettingell W. H., Jung Y.-K., Kovacs D. M., and Tanzi R. E. (1997) Alternative cleavage of Alzheimer-associated presenilins during apoptosis by a caspase-3 family protease. Science 277, 373-376.
40. Kooy N. W., Royall J. A., Ischiropoulos H., and Beckman J. S. (1994) Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radic. Biol. Med. 16, 149-156.
41. Kovacs D. M., Fausett H. J., Page K. J., Kim T.-W., Moir R. D., Merriam D. E., Hollister R. D., Hallmark O. G., Mancini R., Felsenstein K. M., Hyman B. T., Tanzi R. E., and Wasco W. (1996) Alzheimer-associated presenilins 1 and 2: neuronal expression in brain and localization to intracellular membranes in mammalian cells. Nat. Med. 2, 224-229.
42. Kroemer G., Zamzami N., and Susin S. A. (1997) Mitochondrial control of apoptosis. Immunol. Today 18, 44-51.
43. Kruman I., Bruce-Keller A. J., Bredesen D. E., Waeg G., and Mattson M. P. (1997) Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J. Neurosci. 17, 5097-5108.
44. Lafon-Cazal M., Pietri S., Cuicasi M., and Bockaert J. (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364, 535-537.
45. Lehmann S., Chiesa R., and Harris D. A. (1997) Evidence for a six-transmembrane domain structure of presenilin 1. J. Biol. Chem. 272, 12047-12051.
46. Loo D., Copani A., Pike C., Whittemore E., Walencewicz A., and Cotman C. W. (1993) Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
47. Lovell M. A., Ehmann W. D., Mattson M. P., and Markesbery W. R. (1997) Elevated 4-hydroxynonenal in ventricular fluid in Alzheimer's disease. Neurobiol. Aging 18, 457-461.
48. 2+ homeostasis and cell death. J. Neurosci. 15, 6239-6249.
49. Mark R. J., Blanc E. M., and Mattson M. P. (1996) Amyloid β-peptide and oxidative cell injury in Alzheimer's disease. Mol. Neurobiol. 12, 211-224.
50. Mark R. J., Lovell M. A., Markesbery W. R., Uchida K., and Mattson M. P. (1997a) A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68, 255-264.
51. Mark R. J., Pang Z., Geddes J. W., and Mattson M. P. (1997b) Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17, 1046-1054.
52. Mattson M. P. (1990) Antigenic changes similar to those seen in neurofibrillary tangles are elicited by glutamate and calcium influx in cultured hippocampal neurons. Neuron 4, 105-117.
53. Mattson M. P. (1997) Cellular actions of β-umyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol. Rev. 77, 1081-1132.
54. Mattson M. P., Cheng B., Davis D., Bryant K., Lieberburg I., and Rydel R. E. (1992) β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12, 376-389.
55. Mattson M. P., Barger S. W., Cheng B., Lieberburg L. Smith-Swintosky V. L., and Rydel R. E. (1993) β-Amyloid precursor protein metabolites and loss of neuronal calcium homeostasis in Alzheimer's disease. Trends Neurosci. 16, 409-415.
56. Mattson M. P., Goodman Y., Luo H., Fu W., and Furukawa K. (1997a) 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, 681-697.
57. Mattson M. P., Robinson N., and Guo Q. (1997b) Estrogens stabilize mitochondrial function and protect neural cells against the proapoptotic action of mutant presenilin-1. Neuroreport 8, 3817-3821.
58. Mattson M. P., Fu W., Waeg G., and Uchida K. (1997c) 4-Hydroxynonenal, a product of lipid peroxidation, inhibits dephosphorylation of the microtubule-associated protein tau. Neuroreporf 8, 2275-2281.
59. Mattson M. P., Guo Q., Furukawa K., and Pedersen W. A. (1998a) Presenilins, the endoplasmic reticulum, and neuronal apoptosis in Alzheimer's disease. J. Neurochem. 70, 1-14.
60. Mattson M. P., Keller J. N., and Begley J. G. (1998b) Evidence for synaptic apoptosis. Exp. Neurol. 153, 35-48.
61. Mecocci P., MacGarvey M. S., and Beal M. F. (1994) Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 36, 747-751.
62. Miller D. K. (1997) The role of the caspase family of cysteine proteases in apoptosis. Semin. Immunol. 9, 35-49.
63. Otvos L., Szendrei G. I., Lee V. M.-Y., and Mantsch H. H. (1993) Human and rodent Alzheimer β-amyloid peptides acquire distinct conformations in membrane-mimicking solvents. Eur. J. Biochem. 211, 249-257.
64. Qian S., Jiang P., Guan X. M., Singh G., Trumbauer M. E., Yu H., Chen H. Y., Van de Ploeg L. H., and Zheng H. (1998) Mutant human presenilin 1 protects presenilin 1 null mouse against embryonic lethality and elevates Aβ1-42/43 expression. Neuron 20, 611-617.
65. Querfurth H. W. and Selkoe D. J. (1994) Calcium ionophore increases amyloid β peptide production by cultured cells. Biochemistry 33, 4550-4561.
66. Sano M., Ernesto C. Thomas R. G., Klauber M. R., Schaler K., Grundman M., Woodbury P., Growdon J., Cotman C. W., Pfeiffer E., Schneider L. S., and Thal L. J. (1997) A controlled trial of selegiline, α-tocopherol, or both as treatment for Alzheimer's disease. The Alzheimer's Disease Cooperative Study. N. Engl. J. Med 336, 1216-1222.
67. Sayre L. M., Zclasko D. A., Harris P. L. R., Perry G., Salomon R. G., and Smith M. A. (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J. Neurochem. 68, 2092-2097.
68. Scheuner D., Eckman C., Jensen M., Song X., Citron M., Suzuki N., Bird T. D., Hardy J., Hutton M., Kukull W., Larson E., Levy-Lahad E., Viitanen M., Peskind E., Poorkaj P., Schellenberg G., Tanzi R., Wasco W., Lannfelt L., Selkoe D., and Younkin S. (1996) The amyloid β protein deposited in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's, disease. Nat. Med. 2, 864-870.
69. Shen J., Bronson R. T., Chen D. F., Xia W., Selkoe D. J., and Tonegawa S. (1997) Skeletal and CNS defects in presenilin-1-deficient mice. Cell 89, 629-639.
70. Smith C. D., Carney J. M., Starke-Reed P. E., Oliver C. N., Stadtman E. R., Floyd R. A., and Markesbery W. R. (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc. Natl. Acad. Sci. USA 88, 10540-10543.
71. Smith M. A., Harris P. L. R., Sayre L. M., Beckman J. S., and Perry G. (1997) Widespread peroxynitrite-mediated damage in Alzheimer's disease. J. Neurosci. 17, 2653-2657.
72. Stein-Behrens B., Mattson M. P., Chang I., Yeh M., and Sapolsky R. M. (1994) Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. J. Neurosci 14, 5373-5380.
73. Su J. H., Anderson A. J., Cummings B., and Cotman C. W. (1994) Immunocytochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5, 2529-2533.
74. Su J. H., Deng G., and Cotman C. W. (1997) Neuronal DNA damage precedes tangle formation and is associated with up-regulation of nitrotyrosine in Alzheimer's disease brain. Brain Res. 774, 193-199.
75. Tang M. X., Jacobs D., Stern Y., Marder K., Schofield P., Gurland B., Andrews H., and Mayeux R. (1996) Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 348, 429-432.
76. Walter J., Capell A., Grunberg J., Pesold B., Schindzielorz A., Prior R., Podlinsy M. B., Fraser P., St. George-Hyslop P., Selkoe D. J., and Haass C. (1996) The Alzheimer's disease-associated presenilins are differentially phosphorylated proteins located predominantly within the endoplasmic reticulum. Mol. Med. 2, 673-691.
77. Wolozin B., Iwasaki K., Vito P., Ganjei J. K., Lacana E., Sunderland T., Zhao B., Kusiak J. W., Wasco W., and D'Adamio L. (1996) Participation of presenilin 2 in apoptosis: enhanced basal activity conferred by an Alzheimer mutation. Science 274, 1710-1713.
78. Wong P. C., Zheng H., Chen H., Becher M. W., Sirinathsinghji D. J. S., Trumbauer M. E., Chen H. Y., Price D. L., Van der Ploeg L. H. T., and Sisodia S. S. (1997) Presenilin 1 is required for Notch1 and DII1 expression in the paraxial mesoderm. Nature 387, 288-292.
79. Yankner B. A. (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16, 921-932.
80. Yu Z. F., Bruce-Keller A. J., Goodman Y., and Mattson M. P. (1998) Uric acid protects neurons against excitotoxic and metabolic insults in cell culture, and against focal ischemic brain injury in vivo. J. Neurosci. Res. 53, 613-625.