Presynaptic Localization of Neprilysin Contributes to Efficient Clearance of Amyloid-β Peptide in Mouse Brain

Journal of Neuroscience

Volumn 24, Issue 4, 2004, Pages 991-998

  Iwata, Nobuhisa ^a   Mizukami, Hiroaki ^b   Shirotani, Keiro ^a,d   Takaki, Yoshie ^a   Muramatsu, Shin Ichi ^b   Lu, Bao ^c   Gerard, Norma P ^c   Gerard, Craig ^c   Ozawa, Keiya ^b   Saido, Takaomi C ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Adeno associated viral vector; Alzheimer; Amyloid peptide; Axonal transport; Axoplasmic transport; Degradation; Endopeptidase; Gene; Gene transfer; Hippocampus; Perforant path; Presynaptic; Projection

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; MEMBRANE METALLOENDOPEPTIDASE; PARVOVIRUS VECTOR;

AGE; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; GENE TRANSFER; HIPPOCAMPUS; MOUSE; NERVE FIBER TRANSPORT; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSORY NERVE; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONAL TRANSPORT; BRAIN; CELL LINE; DEPENDOVIRUS; DISEASE PROGRESSION; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; HUMANS; MICE; MICE, TRANSGENIC; NEPRILYSIN; NEURONS, AFFERENT; PRESYNAPTIC TERMINALS; SENILE PLAQUES;

EID: 9144266913     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4792-03.2004     Document Type: Article

References (48)

1. Akiyama H, Kondo H, Ikeda K, Kato M, McGeer PL (2001) Immunohistochemical localization of neprilysin in the human cerebral cortex: inverse association with vulnerability to amyloid β-protein (Aβ) deposition. Brain Res 902:277-281.
2. Amaral DG, Witter MP (1995) Hippocampal formation. In: The rat nervous system (Paxinos G, ed), pp 443-493. San Diego: Academic.
3. Barnes K, Turner AJ, Kenny AJ (1988) Electronmicroscopic immunocyto-chemistry of pig brain shows that endopeptidase-24.11 is localized in neuronal membranes. Neurosci Lett 94:64-69.
4. Barnes K, Turner AJ, Kenny AJ (1992) Membrane localization of endopeptidase-24.11 and peptidyl dipeptidase A (angiotensin converting enzyme) in the pig brain: a study using subcellular fractionation and electron microscopic immunocytochemistry. J Neurochem 58:2088-2096.
5. Buttini M, Yu GQ, Shockley K, Huang Y, Jones B, Masliah E, Mallory M, Yeo T, Longo FM, Mucke L (2002) Modulation of Alzheimer-like synaptic and cholinergic deficits in transgenic mice by human apolipoprotein E depends on isoform, aging, and overexpression of amyloid/β peptides but not on plaque formation. J Neurosci 22:10539-10548.
6. Buxbaum JD, Thinakaran G, Koliatsos V, O'Callahan J, Slunt HH, Price DL, Sisodia SS (1998) Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J Neurosci 18:9629-9637.
7. Carson JA, Turner AJ (2002) β-Amyloid catabolism: roles for neprilysin (NEP) and other metallopeptidases? J Neurochem 81:1-8.
8. Chiorini JA, Kim F, Yang L, Kotin RM (1999) Cloning and characterization of adeno-associated virus type 5. J Virol 73:1309-1319.
9. Eckman EA, Watson M, Marlow L, Sambamurti K, Eckman CB (2003) Alzheimer's disease β-amyloid peptide is increased in mice deficient in endothelin-converting enzyme. J Biol Chem 278:2081-2084.
10. Farris W, Mansourian S, Chang Y, Lindsley L, Eckman EA, Frosch MP, Eckman CB, Tanzi RE, Selkoe DJ, Guenette S (2003) Insulin-degrading enzyme regulates the levels of insulin, amyloid/β-protein, and the β-amyloid precursor protein intracellular domain in vivo. Proc Natl Acad Sci USA 100:4162-4167.
11. Fukami S, Watanabe K, Iwata N, Haraoka J, Lu B, Gerard NP, Gerard C, Fraser P, Westaway D, St. George-Hyslop P, Saido TC (2002) Aβ-degrading endopeptidase, neprilysin, in mouse brain: synaptic and axonal localization inversely correlating with Aβ pathology. Neurosci Res 43:39-56.
12. Gomez-Isla T, Price IL, McKeel Jr DW, Morris IC, Growdon JH, Hyman BT (1996) Profound loss of layer 11 entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16:4491-4500.
13. Hama E, Shirotani K, Masumoto H, Sekine-Aizawa Y, Aizawa H, Saido TC (2001) Clearance of extracellular and cell-associated amyloid β peptide through viral expression of neprilysin in primary neurons. J Biochem (Tokyo) 130:721-726.
14. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356.
15. Hartley DM, Walsh DM, Ye CP, Diehl T, Vasquez S, Vassilev PM, Teplow DB, Selkoe DJ (1999) Protofibrillar intermediates of amyloid P-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J Neurosci 19:8876-8884.
16. Hsia AY, Masliah F, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
17. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
18. 1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat Med 6:143-150.
19. Iwata N, Tsubuki S, Takaki Y, Shirotani K, Lu B, Gerard NP, Gerard C, Hama E, Lee H-J, Saido TC (2001) Metabolic regulation of brain Aβ by neprilysin. Science 292:1550-1552.
20. Iwata N, Takaki Y, Fukami S, Tsubuki S, Saido TC (2002) Region-specific reduction of Aβ-degrading endopeptidase, neprilysin, in mouse hippocampus upon aging. J Neurosci Res 70:493-500.
21. Kuo YM, Emmerling MR, Vigo-Pelfrey C, Kasunic TC, Kirkpatrick JB, Murdoch GH, Ball MJ, Roher AE (1996) Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains. J Biol Chem 271:4077-4081.
22. 1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
23. Lazarov O, Lee M, Peterson DA, Sisodia SS (2002) Evidence that synaptically released β-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22:9785-9793.
24. Lu B, Gerard NP, Kolakowski Jr LF, Bozza M, Zurakowski D, Finco O, Carroll MC, Gerard C (1995) Neutral endopeptidase modulation of septic shock. J Exp Med 181:2271-2275.
25. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J (1999) Soluble amyloid β peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155:853-862.
26. Marr RA, Rockenstein E, Mukherjee A, Kindy MS, Hersh LB, Gage FH, Verma IM, Masliah E (2003) Neprilysin gene transfer reduces human amyloid pathology in transgenic mice. J Neurosci 23:1992-1996.
27. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL (1999) Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46:860-866.
28. Miller BC, Eckman EA, Sambamurti K, Dobbs N, Chow KM, Eckman CB, Hersh LB, Thiele DL (2003) Amyloid-β peptide levels in brain are inversely correlated with insulysin activity levels in vivo. Proc Natl Acad Sci USA 100:6221-6226.
29. 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
30. Oefner C, D'Arcy A, Hennig M, Winkler FK, Dale GE (2000) Structure of human neutral endopeptidase (Neprilysin) complexed with phosphoramidon. J Mol Biol 296:341-349.
31. Okada T, Nomoto T, Shimazaki K, Lijun W, Lu Y, Matsushita T, Mizukami H, Urabe M, Hanazono Y, Kume A, Muramatsu S, Nakano I, Ozawa K (2002) Adeno-associated virus vectors for gene transfer to the brain. Methods 28:237-247.
32. 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. Texas: Landes Bioscience.
33. Saido TC, Nakahara H (2003) Proteolytic degradation of Aβ by neprilysin and other peptidases. In: Aβ metabolism and Alzheimer's disease (Saido TC, ed), pp 61-80. Texas: Landes Bioscience.
34. N3(pE), in senile plaques. Neuron 14:457-466.
35. Saito T, Takaki Y, Iwata N, Trojanowski J, Saido TC (2003) Alzheimer's disease, neuropeptides, neuropeptidase, and amyloid-β peptide metabolism. Sci Aging Knowl Environ 2003 3: PE1.
36. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791.
37. Sheng JG, Price DL, 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.
38. Shirotani K, Tsubuki S, Iwata N, Takaki Y, Harigaya W, Maruyama K, Kiryu-Seo S, Kiyama H, Iwata H, Tomita T, Iwatsubo T, Saido TC (2001) Neprilysin degrades both amyloidβ peptides 1-40 and 1-42 most rapidly and efficiently among thiorphan- and phosphoramidon-sensitive endopeptidases. J Biol Chem 276:21895-21901.
39. Sze CI, Troncoso JC, Kawas C, Mouton P, Price DL, Martin LJ (1997) Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neurol 56:933-944.
40. Takaki Y, Iwata N, Tsubuki S, Taniguchi S, Toyoshima S, Lu B, Gerard NP, Gerard C, Lee H-J, Shirotani K, Saido TC (2000) Biochemical identification of the neutral endopeptidase family member responsible for the catabolism of amyloid β peptide in the brain. J Biochem (Tokyo) 128:897-902.
41. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, 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.
42. Turner AJ (1998) Neprilysin. In: Proteolytic enzymes (Barrett AJ, Rawlings ND, Woessner JF, eds), pp 1080-1085. London: Academic.
43. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, Benedek GB, Selkoe DJ, Teplow DB (1999) Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274:25945-25952.
44. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539.
45. Wang HW, Pasternak JF, Kuo H, Ristic H, Lambert MP, Chromy B, Viola KL, Klein WL, Stine WB, Krafft GA, Trommer BL (2002) Soluble oligomers of β amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res 924:133-140.
46. Weninger SC, Yankner BA (2001) Inflammation and Alzheimer disease: the good, the bad, and the ugly. Nat Med 7:527-528.
47. Yasojima K, Akiyama H, McGeer EG, McGeer PL (2001a) Reduced neprilysin in high plaque areas of Alzheimer brain: a possible relationship to deficient degradation of β-amyloid peptide. Neurosci Lett 297:97-100.
48. Yasojima K McGeer EG, McGeer PL (2001b) Relationship between β amyloid peptide generating molecules and neprilysin in Alzheimer disease and normal brain. Brain Res 919:115-121.