Secreted form of amyloid precursor protein enhances basal glucose and glutamate transport and protects against oxidative impairment of glucose and glutamate transport in synaptosomes by a cyclic GMP-mediated mechanism

Journal of Neurochemistry

Volumn 73, Issue 2, 1999, Pages 532-537

  Mattson, Mark P ^a,c   Guo, Zhi Hong ^a   Geiger, Jonathan D ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer's disease; Amyloid peptide; Apoptosis; Excitotoxicity; Lipid peroxidation; Synapse

Indexed keywords

8 BROMO CYCLIC GMP; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; FERROUS ION; GLUCOSE; GLUTAMIC ACID;

ALZHEIMER DISEASE; AMINO ACID TRANSPORT; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; RAT;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ALKALOIDS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; CARBAZOLES; CEREBRAL CORTEX; CYCLIC GMP; ENZYME INHIBITORS; FEMALE; FERROUS COMPOUNDS; GLUCOSE; GLUTAMIC ACID; INDOLES; LIPID PEROXIDATION; NEURONS; NEUROTOXINS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; SYNAPTOSOMES; TRITIUM;

ANIMALIA;

EID: 0344483869     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0730532.x     Document Type: Article

References (40)

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. Barger S. and Mattson M. P. (1995) Secreted form of the Alzheimer's amyloid precursor protein stimulates a membrane-associated guanylate cyclase. Biochem. J. 311, 45-47.
3. Barger S. W., Fiscus R. R., Ruth P., Hofmann F., and Mattson M. P. (1995) Role of cyclic GMP in the regulation of neuronal calcium and survival by secreted forms of β-amyloid precursor. J. Neurochem. 64, 2087-2096.
4. Begley J. G., Duan W., Chan S., Duff K., and Mattson M. P. (1999) Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice. J. Neurochem. 72, 1030-1039.
5. DeKosky S. T., Scheff S. W., and Styren S. D. (1996) Structural correlates of cognition in dementia: quantification and assessment of synapse change. Neurodegeneration 5, 417-421.
6. Doyle E., Bruce M. T., Breen K. C., Smith D. C., Anderton B., and Regan C. M. (1990) Intraventricular infusions of antibodies to amyloid β-protein precursor impair the acquisition of a passive avoidance response in the rat. Neurosci. Lett. 115, 97-102.
7. Fazeli M. S., Breen K., Errington M. L., and Bliss T. V. (1994) Increase in extracellular NCAM and amyloid precursor protein following induction of long-term potentiation in the dentate gyrus of anaesthetized rats. Neurosci. Lett. 169, 77-80.
8. Furukawa K. and Mattson M. P. (1998) Secreted amyloid precursor protein a selectively suppresses NMDA receptor currents in hippocampal neurons: involvement of cyclic GMP. Neuroscience 83, 429-438.
9. + channels and suppression of neuronal activity by secreted β-amyloid precursor protein. Nature 379, 74-78.
10. Furukawa K., Sopher B., Rydel R. E., Begley J. G., Martin G. M., and Mattson M. P. (1996b) Increased activity-regulating and neuro-protective efficacy of α-secretase-derived secreted amyloid precursor protein conferred by a C-terminal heparin-binding domain. J. Neurochem. 67, 1882-1896.
11. Garthwaite G. and Garthwaite J. (1988) Cyclic GMP and cell death in rat cerebellar slices. Neuroscience 26, 321-326.
12. 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.
13. Guo Q., Robinson N., and Mattson M. P. (1998) 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.
14. 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 knock-in mice. Nat. Med. 5, 101-107.
15. Huber G., Martin J. R., Loffler J., and Moreau J. L. (1993) Involvement of amyloid precursor protein in memory formation in the rat: an indirect antibody approach. Brain Res. 603, 348-352.
16. Ishida A., Furukawa K., Keller J. N., and Mattson M. P. (1997) Secreted form of β-amyloid precursor protein shifts the frequency dependence for induction of LTD, and enhances LTP in hippocampal slices. Neuroreport 8, 2133-2137.
17. Jin L., Ninomiya H., Roch J., Schubert D., Masliah E., Otero D., and Saitoh T. (1994) Peptides containing the RERMS sequence of amyloid beta/A4 protein precursor bind cell surface and promote neurite extension. J. Neurosci. 14, 5461-5470.
18. 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.
19. Koo E., Sisodia S., Acher D., Martin L., Weidemann A., Beyreuther K., Masters C., Fisher P., and Price D. L. (1990) Precursor of amyloid protein in Alzheimer's disease undergoes fast anterograde axonal transport. Proc. Natl. Acad. Sci. USA 87, 1561-1565.
20. Lannfelt L., Basun H., Wahlund L. O., Rowe B. A., and Wagner S. L. (1995) Decreased α-secretase-cleaved amyloid precursor protein as a diagnostic marker for Alzheimer's disease. Nat. Med. 1, 829-832.
21. 2+ homeostasis and cell death. J. Neurosci. 15, 6239-6249.
22. Mark R. J., Pang Z., Geddes J. W., Uchida K., and Mattson M. P. (1997) Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17, 1046-1054.
23. Masliah E., Raber J., Alford M., Mallory M., Mattson M. P., Yang D., Wong D., and Mucke L. (1998) Amyloid precursor protein stimulates excitatory amino acid transport: implications for neuroprotective in vivo functions. J. Biol. Chem. 273, 12548-12557.
24. Mattson M. P. (1994) Secreted forms of β-amyloid precursor protein modulate dendrite outgrowth and calcium responses to glutamate in cultured embryonic hippocampal neurons. J. Neurobiol. 25, 439-450.
25. Mattson M. P. (1997) Cellular actions of β-amyloid precursor protein, and its soluble and fibrillogenic peptide derivatives. Physiol. Rev. 77, 1081-1132.
26. Mattson M. P., Cheng B., Culwell A. R., Esch F., Lieberburg I., and Rydel R. E. (1993) Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of β-amyloid precursor protein. Neuron 10, 243-254.
27. Mattson M. P., Keller J. N., and Begley J. G. (1998a) Evidence for synaptic apoptosis. Exp. Neurol. 153, 35-48.
28. Mattson M. P., Partin J., and Begley J. G. (1998b) Amyloid β-peptide induces apoptosis-related events in synapses and dendrites. Brain Res. 807, 167-176.
29. Mucke L., Masliah E., Johnson W. B., Ruppe M. D., Alford M., Rockenstein E. M., Rorss-Petter S., Pietropaolo M., Mallory M., and Abraham C. R. (1994) Synaptotrophic effects of human amyloid β protein precursor in the cortex of transgenic mice. Brain Res. 666, 151-167.
30. Nitsch R., Farber A. S., Growdon H. J., and Wurtman J. R. (1993) Release of amyloid β-protein precursor derivatives by electrical depolarization of rat hippocampal slices. Proc. Natl. Acad. Sci. USA 90, 5191-5193.
31. Palmert M. R., Usiak M., Mayeux B., Raskind M., Tourtellotte W. W., and Younkin S. G. (1990) Soluble derivatives of the β-amyloid protein precursor in cerebrospinal fluid: alterations in normal aging and in Alzheimer's disease. Neurology 40, 1028-1034.
32. Roch J.-M., Masliah E., Roch-Levecq A., Sundsmo M., Otero D. A., Veinbergs I., and Saitoh T. (1994) Increase of synaptic density and memory retention by a peptide representing the trophic domain of the amyloid β/A4 protein precursor. Proc. Natl. Acad. Sci. USA 91, 7450-7454.
33. Schubert W., Prior R., Weidemann A., Dircksen H., Multhaup G., Masters C., and Beyreuther K. (1991) Localization of Alzheimer βA4 amyloid at presynaptic terminals. Brain Res. 563, 184-194.
34. Shanahan M. F. and Edwards B. M. (1989) Stimulation of glucose transport in rat cardiac myocytes by guanosine 3′,5′-monophosphate. Endocrinology 125, 1074-1081.
35. 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.
36. 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.
37. Smith M. A., Hirai K., Hsiao K., Pappolla M. A., Harris P. L. R., Siedlak S. L., Tabaton M., and Perry G. (1998) Amyloid-β deposition in Alzheimer transgenic mice is associated with oxidative stress. J. Neurochem. 70, 2212-2215.
38. Smith-Swintosky V. L., Pettigrew L. C., Craddock S. D., Culwell A. R., Rydel R. E., and Mattson M. P. (1994) Secreted forms of β-amyloid precursor protein protect against ischemic brain injury. J. Neurochem. 63, 781-784.
39. Terry R. D., Masliah E., Salmon D. P., Butters N., DeTeresa R., Hill R., Hansen L. A., and Katzman R. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580.
40. Young M. E., Radda G. K., and Leighton B. (1997) Nitric oxide stimulates glucose transport and metabolism in rat skeletal muscle in vitro. Biochem. J. 322, 223-228.