Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice

Journal of Neurochemistry

Volumn 72, Issue 3, 1999, Pages 1030-1039

  Begley, James G ^a   Duan, Wenzhen ^a   Chan, Sic ^a   Duff, Karen ^b   Mattson, Mark P ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer's disease; Amyloid; Apoptosis; Caspase; Depolarization; Reactive oxygen species; Synaptosomes

Indexed keywords

CALCIUM; PRESENILIN 1; REACTIVE OXYGEN METABOLITE;

ADOLESCENT; ALZHEIMER DISEASE; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN MITOCHONDRION; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; ENZYME ACTIVATION; GENE MUTATION; MALE; MEMBRANE DEPOLARIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNAPTOSOME; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; BLOTTING, WESTERN; CALCIUM; CASPASE 3; CASPASES; CEREBRAL CORTEX; CHELATING AGENTS; CYTOPLASM; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GENOTYPE; HOMEOSTASIS; MALE; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; MUTATION; PRESENILIN-1; SYNAPSES; SYNAPTOSOMES;

ANIMALIA; MUS MUSCULUS;

EID: 0032972922     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0721030.x     Document Type: Article

References (72)

1. Ancolio K., Marambaud P., Dauch P., and Checler F. (1997) α-Secretase-derived product of β-amyloid precursor prolein is decreased by presenilin 1 mutations linked to familial Alzheimer's disease. J. Neurochem. 69, 2494-2499.
2. Beal M. F. (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Ann. Neurol. 38, 357-366.
3. Beal M. F., Brouillet E., Jenkins B., Ferrante R., Kowall N. W., Miller J., Storey E., Srivastava R., Rosen B. R., and Hyman B. T. (1993) Neurochemical and histological characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J. Neurosci. 13, 4181-4192.
4. 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.
5. Citron M., Westaway D., Xia W., Carlson G., Diehl T., Levesque G., Johnson-Wood K., Lee M., Seubert P., Davis A., Kholodenko D., Motter R., Sherrington R., Perry B., Yao H., Strome R., Lieberburg I., Rommens J., Kim S., Schenk D., Fraser P., St. George Hyslop P., and Selkoe D. J. (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid β-protein in both transfected cells and transgenic mice. Nat. Med. 3, 67-72.
6. Cook D. B., Sung J. C., Golde T. E., Felsenstein K. M., Wojczyk B. S., Tanzi R. E., Trojanowski J. Q., Lee V. M. Y., and Doms R. W. (1996) Expression and analysis of presenilin 1 in a human neuronal system: localization in cell bodies and dendrites. Proc. Natl. Acad. Sci. USA 93, 9223-9228.
7. Cotman C. W. and Anderson A. J. (1995) A potential role for apoptosis in neurodegeneration and Alzheimer's disease. Mol. Neurobiol. 10, 19-45.
8. Cotman C. W. and Matthews D. A. (1971) Synaptic plasma membranes from rat brain synaptosomes: isolation and partial characterization. Biochim. Biophys. Acta 249, 380-394.
9. 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.
10. De Strooper B., Beullens M., Contreras B., Levesque L., Craessaerts K., Cordell B., Moechars D., Bollen M., Fraser P., St. George-Hyslop P. S., and Van Leuven F. (1997) Phosphorylation, subcellular localization, and membrane orientation of the Alzheimer's disease-associated presenilins. J. Biol. Chem. 272, 3590-3598.
11. Doan A., Thinakaran G., Borchelt D. R., Slunt H. H., Ratovitsky 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.
12. 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.
13. Elder G. A., Tezapsidis N., Carter J., Shioi J., Bouras C., Li D., Johnston J. M., Efthimiopoulos S., Friedrich V. L., and Robakis N. K. (1996) Identification and neuron specific expression of the S182/presenilin 1 protein in human and rodent brains. J. Neurosci. Res. 45, 308-320.
14. Fukuyama R., Wadhwani K. C., Galdzicki Z., Rapoport S. I., and Ehrenstein G. (1994) β-Amyloid polypeptide increases calcium-uptake in PC12 cells: a possible mechanism for its cellular toxicity in Alzheimer's disease. Brain Res. 667, 269-272.
15. Furukawa K., Sopher B. L., Rydel R. E., Begley J. G., Pham D. 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 is conferred by a C-terminal heparin-binding domain. J. Neurochem. 67, 1882-1896.
16. Furukawa K., Guo Q., Schellenberg G. D., and Mattson M. P. (1998) Presenilin-1 mutation alters NGF-induced neunte outgrowth, calcium homeostasis, and transcription factor (AP-1) activation in PC12 cells. J. Neurosci. Res. 52, 618-624.
17. 2+ changes in rat cortical synaptosomes. J. Neurochem. 53, 392-398.
18. Goodman Y. and Mattson M. P. (1994) Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peplide-induced oxidative injury. Exp. Neurol. 128, 1-12.
19. Gordon-Weeks P. R., Burgoyne R. D., and Gray E. G. (1982) Presynaptic microtubules: organisation and assembly/disassembly. Neuroscience 7, 739-749.
20. Guo Q., Furukawa K., Sopher B. L., Pham D. G., Xie J., Robinson N., Martin G. M., and Maltson 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.
21. 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.
22. Guo Q., Robinson N., and Mattson M. P. (1998a) 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.
23. Guo Q., Christakos S., Robinson N., and Mattson M. P. (1998b) 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.
24. Guo Q., Fu W., Xie J., Luo H., Sells S. F., Geddes J. W., Bondada V., Rangnekar V., and Mattson M. P. (1998c) Par-4 is a mediator of neuronal degeneration associated with the pathogenesis of Alzheimer's disease. Nat. Med. 4, 957-962.
25. Guo Q., Sebastian L., Sopher B. L., Miller M. W., Ware C. B., Martin G. M., and Mattson M. P. (1999a) 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. J. Neurochem. 72, 1019-1029.
26. Guo Q., Fu W., Sopher B. L., Miller M. W., Ware C. B., Martin G. M., and Mattson M. P. (1999b) Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knockin mice. Nat. Med. 5 (in press).
27. Hardy J. (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci. 20, 154-159.
28. Hoth M., Fanger C. M., and Lewis R. S. (1997) Mitochondrial regulation of store operated calcium signaling in T lymphocytes. J. Cell Biol. 137, 633-648.
29. 2+ mobilization is altered in fibroblasts from patients with Alzheimer's disease. Proc. Natl. Acad. Sci. USA 91, 534-538.
30. Juin P., Pelletier M., Oliver L., Tremblais K., Gregoire M., Meflah K., and Vallette F. M. (1998) Induction of a caspase-3-like activity by calcium in normal cytosolic extracts triggers nuclear apoptosis in a cell-free system. J. Biol. Chem. 273, 17559-17564.
31. Kaneko I., Yamada N., Sakuraba Y., Kamenosono M., and Tutumi S. (1995) Suppression of mitochondrial succinate dehydrogenase, a primary target of β-amyloid, and its derivative racemized at Ser residue. J. Neurochem. 65, 2585-2593.
32. 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.
33. Keller J. N., Guo Q., Holtsberg F. W., Bruce-Keller A. J., and Mattson M. P. (1998a) Increased sensitivity to mitochondrial toxin-induced apoptosis in neural cells expressing mutant presenilin-1 is linked to perturbed calcium homeostasis and enhanced oxyradical production. J. Neurosci. 18, 4439-4450.
34. 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. (1998b) Mitochondrial MnSOD prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation and mitochondrial dysfunction. J. Neurosci. 18, 687-697.
35. Kim T. W. and Tanzi R. E. (1997) Presenilins and Alzheimer's disease. Curr. Opin. Neurobiol. 7, 683-688.
36. Koh J., Yang L. L., and Cotman C. W. (1990) Beta-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res. 533, 315-320.
37. 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.
38. Kruman I. and Mattson M. P. (1998) Pivotal role of mitochondrial calcium uptake in neural cell apoptosis and necrosis. J. Neurochem. 72, 529-540.
39. Kruman I., Guo Q., and Mattson M. P. (1998) Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. J. Neurosci. Res. 51, 293-308.
40. Lassmann H., Fischer P., and Jellinger K. (1993) Synaptic pathology of Alzheimer's disease. Ann. NY Acad. Sci. 695, 59-64.
41. 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.
42. Levitan D. and Greenwald I. (1995) Facilitation of lin-12-mediated signaling by sel-12, a Caenorhabditis elegans S182 Alzheimer's disease gene. Nature 377, 351-354.
43. Luo Y., Sunderland T., and Wolozin B. (1996) Physiologic levels of β-amyloid activate phosphatidylinositol 3-kinase with the involvement of tyrosine phosphorylation. J. Neurochem. 67, 978-987.
44. 2+ homeostasis and cell death. J. Neurosci. 15, 6239-6249.
45. Mark R. J., Lovell M. A., Markesberry W. R., Uchida K., and Mattson M. P. (1997a) A role for 4-hydroxynonenal in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68, 255-264.
46. +-ATPases activity in hippocampal neurons. Brain Res. 756, 205-214.
47. Mattson M. P. (1998) Experimental models of Alzheimer's disease. Sci. Med. March/April, pp. 16-25.
48. 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.
49. Mattson M. P., Tomaselli K., and Rydel R. E. (1993a) Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res. 621, 35-49.
50. Mattson M. P., Cheng B., Culwell A., Esch F., Lieberburg I., and Rydel R. E. (1993b) Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of β-amyloid precursor protein. Neuron 10, 243-254.
51. Mattson M. P., Furukawa K., Bruce A. J., Mark R. J., and Blanc E. (1996) Calcium homeostasis and free radical metabolism as convergence points in the pathophysiology of dementia, in Molecular Mechanisms of Dementia (Wasco W. and Tanzi R. E., eds), pp. 103-143. Humana Press, Totowa, New Jersey.
52. 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.
53. Mattson M. P., Keller J. N., and Begley J. G. (1998b) Evidence for synaptic apoptosis. Exp. Neurol. 153, 35-48.
54. Mattson M. P., Partin J., and Begley J. G. (1998c) Amyloid β-peptide induces apoptosis-related events in synapses and dendrites. Brain Res. 807, 167-176.
55. Mercken M., Takahashi H., Honda T., Sato K., Murayama M., Nakazato Y., Noguchi K., Imahori K., and Takashima A. (1996) Characterization of human presenilin 1 using N-terminal specific monoclonal antibodies: evidence that Alzheimer mutations affect proteolytic processing. FEBS Lett. 389, 297-303.
56. Nixon R. A., Saito K. I., Grynspan F., Griffin W. R., Katayama S., Honda T., Mohan P. S., Shea T. B., and Beermann M. (1994) Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer's disease. Ann. NY Acad. Sci. 747, 77-91.
57. 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.
58. Pedersen W. A., Kloczewiak M. A., and Blusztajn J. K. (1996) Amyloid β-protein reduces acetylcholine synthesis in a cell line derived from cholinergic neurons of the basal forebrain. Proc. Natl. Acad. Sci. USA 93, 8068-8071.
59. Pedersen W. A., Guo Q., Hartman B. K., and Mattson M. P. (1997) Nerve growth factor-independent reduction in choline acetyltransferase activity in PC12 cells expressing mutant presenilin-1. J. Biol. Chem. 272, 22397-22400.
60. Pike C. J., Burdick D., Walencewicz A. J., Glabe C. G., and Cotman C. W. (1993) Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13, 1676-1687.
61. 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.
62. 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) Secreted amyloid β-protein similar to that 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.
63. 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.
64. Spacek J. and Harris K. M. (1997) Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17, 190-203.
65. Takadera T. and Ohyashiki T. (1997) Apoptotic cell death and caspase 3 (CPP32) activation induced by calcium ionophore at low concentrations and their prevention by nerve growth factor in PC12 cells. Eur. J. Biochem. 249, 8-12.
66. Thinakaran G., Borchelt D. R., Lee M. K., Slunt H. H., Spitzer L., Kim G., Ratovitsky T., Davenport F., Norstedt C., Seeger M., Hardy J., Levey A., Gandy S. E., Jenkins N. A., Copeland N. G., Price D. L., and Sisodia S. A. (1996) Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17, 181-190.
67. 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.
68. Walter J., Grunberg J., Schindzielorz A., and Haass C. (1998) Proteolytic fragments of the Alzheimer's disease associated presenilins-1 and -2 are phosphorylated in vivo by distinct cellular mechanisms. Biochemistry 37, 5961-5967.
69. Weidemann A., Paliga K., Durrwang U., Czech C., Evin G., Masters C. L., and Beyreuther K. (1997) Formation of stable complexes between two Alzheimer's disease gene products: presenilin-2 and β-amyloid precursor protein. Nat. Med. 3, 328-332.
70. 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 Dll1 expression in the paraxial mesoderm. Nature 387, 288-292.
71. Xia W., Zhang J., Perez R., Koo E. H., and Selkoe D. J. (1997) Interaction between amyloid precursor protein and presenilins in mammalian cells: implications for the pathogenesis of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 94, 8208-8213.
72. Yankner B. A. (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16, 921-932.