Inhibition of neprilysin by infusion of thiorphan into the hippocampus causes an accumulation of amyloid β and impairment of learning and memory

Journal of Pharmacology and Experimental Therapeutics

Volumn 317, Issue 1, 2006, Pages 334-340

  Zou, Li Bo ^a   Mouri, Akihiro ^b   Iwata, Nobuhisa ^c   Saido, Takaomi C ^c   Wang, Dayong ^b   Wang, Min Wei ^a   Mizoguchi, Hiroyuki ^b   Noda, Yukihiro ^b,d   Nabeshima, Toshitaka ^b  

^a SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^d MEIJO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; MEMBRANE METALLOENDOPEPTIDASE; NICOTINE; THIORPHAN;

ACETYLCHOLINE RELEASE; ALZHEIMER DISEASE; ARTICLE; CATABOLISM; CHOLINERGIC ACTIVITY; CONDITIONING; CONTROLLED STUDY; HIPPOCAMPUS; INFUSION; LEARNING; LEARNING DISORDER; LOCOMOTION; MALE; MAZE TEST; MEMORY; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; STATISTICAL ANALYSIS;

ACETYLCHOLINE; AMYLOID BETA-PROTEIN; ANIMALS; ENZYME INHIBITORS; HIPPOCAMPUS; INFUSIONS, PARENTERAL; MALE; MAZE LEARNING; MEMORY; MOTOR ACTIVITY; NEPRILYSIN; NICOTINE; PEPTIDE FRAGMENTS; RATS; RATS, WISTAR; THIORPHAN;

EID: 33645114238     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.105.095687     Document Type: Article

References (39)

1. Ainge JA, Heron-Maxwell C, Theofilas P, Wright P, de Hoz L, and Wood ER (2006) The role of the hippocampus in object recognition in rats: examination of the influence of task parameters and lesion size. Behav Brain Res 167:183-195.
2. Dolev I and Michaelson DM (2004) A nontransgenic mouse model shows inducible amyloid-β (Aβ) peptide deposition and elucidates the role of apolipoprotein E in the amyloid cascade. Proc Natl Acad Sci USA 101:13909-13914.
3. Eckman EA, Watson M, Malow L, Sambamurti K, and Eckman CB (2003) Alzheimer's disease β-amyloid peptide is increased in mice deficient in endothelin-converting enzyme. J Biol Chem 278:2081-2084.
4. Ennaceur A, Neave N, and Aggleton JP (1996) Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80:9-25.
5. Farris W, Mansourian S, Chang Y, Lindsley L, Eckman EA, Frocsh MP, Eckman CB, Tanzi RE, Selkoe DJ, and Guenette S (2003) Insulin degrading enzyme regulates the levels of insulin, amyloid-β protein, β-amyloid precursor protein intracellular domain in vivo. Proc Natl Acad Sci USA 100:4162-4167.
6. Fukami S, Watanabe K, Iwata N, Haraoka J, Lu B, Gerard NP, Gerard C, Fraser P, Westaway D, St George-Hyslop P, et al. (2002) Aβ-degrading endopeptidase, neprilysin, in mouse brain: synaptic and axonal localization inversely correlating with Aβ pathology. Neurosci Res 43:39-56.
7. Gallagher M, King RA, and Young NB (1983) Opiate antagonists improve spatial memory. Science (Wash DC) 221:975-976.
8. Hardy J and Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science (Wash DC) 297:353-356.
9. Itoh A, Akaike T, Sokabe M, Nitta A, Iida R, Olariu A, Yamada K, and Nabeshima T (1999) Impairments of long-term potentiation in hippocampal slices of β-amyloid-infused rats. Eur J Pharmacol 382:167-175.
10. Iwata N, Higuchi H, and Saido TC (2005) Metabolism of amyloid β peptide and Alzheimer's disease. Pharmacol Ther 108:129-148.
11. Iwata N, Mizukami H, Shirotani K, Takaki Y, Muramatsu S, Lu B, Gerard NP, Gerard C, Ozawa K and Saido. TC (2004) Presynaptic localization of neprilysin contributes to efficient clearance of amyloid-β peptide in mouse brain. J Neurosci 24:991-998.
12. Iwata N, Takaki Y, Fukami S, Tsubuki S, and Saido TC (2002) Region-specific reduction of Aβ-degrading endopeptidase, neprilysin, in mouse hippocampus upon aging. J Neurosci Res 70:493-500.
13. Iwata N, Tsubuki S, Takaki Y, Shirotani K, Lu B, Gerard NP, Gerard C, Hama E, Lee HJ, and Saido TC (2001) Metabolic regulation of brain Aβ by neprilysin. Science (Wash DC) 292:1550-1552.
14. 1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat Med 6:143-150.
15. Janak PH and Martinez JL Jr (1990) Only tyrosine-containing metabolites of [Leu]enkephalin impair active avoidance conditioning in mice. Pharmacol Biochem Behav 37:655-659.
16. Jarrett JT, Berger EP, and Lansbury PT Jr (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32:4693-4697.
17. Kanemitsu H, Tomiyama T, and Mori H (2003) Human neprilysin is capable of degrading amyloid β peptide not only in the monomeric form but also the pathological oligomeric form. Neurosci Lett 350:113-116.
18. Lazarov O, Lee M, Peterson DA, and Sisodia SS (2002) Evidence that synaptically released β-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22:9785-9793.
19. Lazarov O, Robinson J, Tang YP, Hairston IS, Korade-Mirnics Z, Lee VM, Hersh LB, Sapolsky RM, Mirnics K, and Sisodia SS (2005) Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell 120:701-713.
20. Leissring MA, Farris W, Chang AY, Walsh DM, Wu X, Sun X, Frosch MP, and Selkoe DJ (2003) Enhanced proteolysis of β-amyloid in APP transgenic mice prevents plaque formation, secondary pathology and premature death. Neuron 40:1087-1093.
21. Morris RG, Garrud P, Rawlins JN, and O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature (Lond) 297:681-683.
22. Nitta A, Itoh A, Hasegawa T, and Nabeshima T (1994) β-Amyloid protein-induced Alzheimer's disease animal model. Neurosci Lett 170:63-66.
23. Paxinos G and Watson C (1986) The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego.
24. Phillips RG and LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
25. Ramirez-Alvarado M, Merkel JS, and Regan L (2000) A systematic exploration of the influence of the protein stability on amyloid fibril formation in vitro. Proc Natl Acad Sci USA 97:8979-8984.
26. Saido TC (2003) Overview-Aβ metabolism: from Alzheimer research to brain aging control, in Aβ Metabolism and Alzheimer's Disease (Saido TC ed) pp 1-16, Landes Bioscience, Georgetown, TX.
27. Saido TC and Nakahara H (2003) Proteolytic degradation of Aβ by neprilysin and other peptidases, in Aβ Metabolism and Alzheimer's Disease (Saido TC eds) pp 61-80, Landes Bioscience, Georgetown, TX.
28. Saito T, Iwata N, Tsubuki S, Takaki Y, Takano J, Huang SM, Suemoto T, Higuchi M, and Saido TC (2005) Somatostatin regulates brain amyloid β peptide Aβ42 through modulation of proteolytic degradation. Nat Med 11:434-439.
29. Saito T, Takaki Y, Iwata N, Trojanowski J, and Saido TC (2003) Alzheimer's disease, neuropeptides, neuropeptidase and amyloid-β peptide metabolism. Sci Aging Knowl Environ 2003(3):PE1.
30. Saria A, Hauser KF, Traurig HH, Turbek CS, Hersh L, and Gerard C (1997) Opioid-related changes in nociceptive threshold and in tissue levels of enkephalins after target disruption of the gene for neutral endopeptidase (EC 3.4.24.11) in mice. Neurosci Lett 234:27-30.
31. Selkoe DJ and Schenk D (2003) Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43:545-584.
32. Sheng JG, Price DL, and Koliatsos VE (2002) Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Aβ amyloidosis. J Neurosci 22:9794-9799.
33. Suh YH and Checler F (2002) Amyloid precursor protein, presenilins and α-synuclein: molecular pathogenesis and pharmacological applications in Alzheimer's disease. Pharmacol Rev 54:469-525.
34. Tran MH, Yamada K, Nakajima A, Mizuno M, He J, Kamei H, and Nabeshima T (2003) Tyrosine nitration of a synaptic protein synaptophysin contributes to amyloid β-peptide-induced cholinergic dysfunction. Mol Psychiatry 8:407-412.
35. Turner AJ and Tanzawa K (1997) Mammalian membrane metallopeptidases: NEP, ECE, KELL and PEX. FASEB J 11:355-364.
36. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, et al. (1999) B-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science (Wash DC) 286:735-741.
37. Yamada K, Tanaka T, Han D, Senzaki K, Kameyama T, and Nabeshima T (1999) Protective effects of idebenone and α-tocopherol on β-amyloid-(1-42)- induced learning and memory deficits in rats: implication of oxidative stress in β-amyloid-induced neurotoxicity in vivo. Eur J Neurosci 11:83-90.
38. Yasojima K, Akiyama H, McGeer EG, and McGeer PL (2001) Reduced neprilysin in high plaque areas of Alzheimer brain: a possible relationship to deficient degradation of β-amyloid peptide. Neurosci Lett 297:97-100.
39. Zhang Z, Nadeau P, Song W, Donoviel D, Yuan M, Bernstein A, and Yankner BA (2000) Presenilins are required for γ-secretase cleavage of β-APP and transmembrane cleavage of Notch-1. Nat Cell Biol 2:463-465.