Long-term neprilysin gene transfer is associated with reduced levels of intracellular Abeta and behavioral improvement in APP transgenic mice

BMC Neuroscience

Volumn 9, Issue , 2008, Pages

  Spencer, Brian ^a   Marr, Robert A ^c   Rockenstein, Edward ^a,b   Crews, Leslie ^b   Adame, Anthony ^a   Potkar, Rewati ^a   Patrick, Christina ^a   Gage, Fred H ^d   Verma, Inder M ^a,b   Masliah, Eliezer ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

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

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER; IMMUNOREACTIVITY; MAZE TEST; MOUSE; NERVE DEGENERATION; NONHUMAN; PROTEIN AGGREGATION; TRANSGENIC MOUSE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; BIOSYNTHESIS; BRAIN; DISEASE MODEL; GENETICS; HUMAN; INTRACELLULAR FLUID; LENTIVIRINAE; METABOLISM; METHODOLOGY; NERVE CELL; PATHOLOGY; SENILE PLAQUE; TIME;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; INTRACELLULAR FLUID; LENTIVIRUS; MAZE LEARNING; MICE; MICE, TRANSGENIC; NEPRILYSIN; NEURONS; SENILE PLAQUES; TIME;

EID: 57449117668     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-9-109     Document Type: Article

References (72)

1. Ashford JW APOE genotype effects on Alzheimer's disease onset and epidemiology J Mol Neurosci 2004, 23(3):157-165. 15181244 15181244
2. Masliah E The role of synaptic proteins in Alzheimer's disease Ann N Y Acad Sci 2000, 924:68-75. 11193804
3. Selkoe DJ Alzheimer's disease is a synaptic failure Science 2002, 298(5594):789-791. 12399581 12399581
4. DeKosky S Scheff S Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity AnnNeurol 1990, 27:457-464. 2360787
5. Mucke L Masliah E Yu GQ Mallory M Rockenstein EM Tatsuno G Hu K Kholodenko D Johnson-Wood K McConlogue L High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation J Neurosci 2000, 20(11):4050-4058. 10818140 10818140
6. Selkoe DJ Amyloid beta-protein precursor: New clues to the genesis of Alzheimer's disease Curr Opin Neurobiol 1994, 4(5):708-716. 7849528 7849528
7. Glabe CC Amyloid accumulation and pathogensis of Alzheimer's disease: significance of monomeric, oligomeric and fibrillar Abeta Subcell Biochem 2005, 38:167-177. 15709478 15709478
8. Klein WL Krafft GA Finch CE Targeting small Abeta oligomers: The solution to an Alzheimer's disease conundrum? Trends Neurosci 2001, 24(4):219-224. 11250006 11250006
9. Selkoe DJ Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior Behav Brain Res 2008, 192(1):106-113. 18359102
10. Cuello AC Canneva F Impact of intracellular beta-amyloid in transgenic animals and cell models Neurodegener Dis 2008, 5(3-4):146-148. 18322374 18322374
11. Cuello AC Intracellular and extracellular Abeta, a tale of two neuropathologies Brain Pathol 2005, 15(1):66-71. 15779238 15779238
12. LaFerla FM Green KN Oddo S Intracellular amyloid-beta in Alzheimer's disease Nat Rev Neurosci 2007, 8(7):499-509. 17551515 17551515
13. Lee EK Park YW Shin DY Mook-Jung I Yoo YJ Cytosolic amyloid-beta peptide 42 escaping from degradation induces cell death Biochem Biophys Res Commun 2006, 344(2):471-477. 16630565 16630565
14. Spencer B Rockenstein E Crews L Marr R Masliah E Novel strategies for Alzheimer's disease treatment Expert Opin Biol Ther 2007, 7(12):1853-1867. 18034651 18034651
15. Cai H Wang Y McCarthy D Wen H Borchelt DR Price DL Wong PC BACE1 is the major beta-secretase for generation of Abeta peptides by neurons Nat Neurosci 2001, 4(3):233-234. 11224536
16. Luo JJ Wallace W Riccioni T Ingram DK Roth GS Kusiak JW Death of PC12 cells and hippocampal neurons induced by adenoviral-mediated FAD human amyloid precursor protein gene expression J Neurosci Res 1999, 55(5):629-642. 10082085 10082085
17. Schapira AH Etiology of Parkinson's disease Neurology 2006, 66(10 Suppl 4):S10-23. 16717248
18. Vassar R Bennett BD Babu-Khan S Kahn S Mendiaz EA Denis P Teplow DB Ross S Amarante P Loeloff R et al.: Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE Science 1999, 286(5440):735-741. 10531052 10531052
19. Sinha S Anderson JP Barbour R Basi GS Caccavello R Davis D Doan M Dovey HF Frigon N Hong J et al.: Purification and cloning of amyloid precursor protein beta-secretase from human brain Nature 1999, 402(6761):537-540. 10591214 10591214
20. Howell S Nalbantoglu J Crine P Neutral endopeptidase can hydrolyze beta-amyloid(1-40) but shows no effect on beta-amyloid precursor protein metabolism Peptides 1995, 16(4):647-652. 7479298 7479298
21. Iwata N Tsubuki S Takaki Y Watanabe K Sekiguchi M Hosoki E Kawashima-Morishima M Lee HJ Hama E Sekine-Aizawa Y et al.: Identification of the major Abeta1-42-degrading catabolic pathway in brain parenchyma: Suppression leads to biochemical and pathological deposition Nat Med 2000, 6(2):143-150. 10655101 10655101
22. Iwata N Tsubuki S Takaki Y Shirotani K Lu B Gerard NP Gerard C Hama E Lee HJ Saido TC Metabolic regulation of brain Abeta by neprilysin Science 2001, 292(5521):1550-1552. 11375493 11375493
23. Akiyama H Kondo H Ikeda K Kato M McGeer PL Immunohistochemical localization of neprilysin in the human cerebral cortex: Inverse association with vulnerability to amyloid beta-protein (Abeta) deposition Brain Res 2001, 902(2):277-281. 11384622 11384622
24. Reilly CE Neprilysin content is reduced in Alzheimer brain areas J Neurol 2001, 248(2):159-160. 11284139
25. Caccamo A Oddo S Sugarman MC Akbari Y LaFerla FM Age- and region-dependent alterations in Abeta-degrading enzymes: Implications for Abeta-induced disorders Neurobiol Aging 2005, 26(5):645-654. 15708439 15708439
26. Yasojima K McGeer EG McGeer PL Relationship between beta amyloid peptide generating molecules and neprilysin in Alzheimer disease and normal brain Brain Res 2001, 919(1):115-121. 11689168 11689168
27. Yasojima K Akiyama H McGeer EG McGeer PL Reduced neprilysin in high plaque areas of Alzheimer brain: A possible relationship to deficient degradation of beta-amyloid peptide Neurosci Lett 2001, 297(2):97-100. 11121879 11121879
28. Apelt J Ach K Schliebs R Aging-related down-regulation of neprilysin, a putative beta-amyloid-degrading enzyme, in transgenic Tg2576 Alzheimer-like mouse brain is accompanied by an astroglial upregulation in the vicinity of beta-amyloid plaques Neurosci Lett 2003, 339(3):183-186. 12633883 12633883
29. Maruyama M Higuchi M Takaki Y Matsuba Y Tanji H Nemoto M Tomita N Matsui T Iwata N Mizukami H et al.: Cerebrospinal fluid neprilysin is reduced in prodromal Alzheimer's disease Ann Neurol 2005, 57(6):832-842. 15929037 15929037
30. Wang DS Lipton RB Katz MJ Davies P Buschke H Kuslansky G Verghese J Younkin SG Eckman C Dickson DW Decreased neprilysin immunoreactivity in Alzheimer disease, but not in pathological aging J Neuropathol Exp Neurol 2005, 64(5):378-385. 15892294
31. Oda M Morino H Maruyama H Terasawa H Izumi Y Torii T Sasaki K Nakamura S Kawakami H Dinucleotide repeat polymorphisms in the neprilysin gene are not associated with sporadic Alzheimer's disease Neurosci Lett 2002, 320(1-2):105-107. 11849775
32. Sodeyama N Mizusawa H Yamada M Itoh Y Otomo E Matsushita M Lack of association of neprilysin polymorphism with Alzheimer's disease and Alzheimer's disease-type neuropathological changes J Neurol Neurosurg Psychiatry 2001, 71(6):817-818. 1737626 11762318
33. Shi J Zhang S Tang M Ma C Zhao J Li T Liu X Sun Y Guo Y Han H et al.: Mutation screening and association study of the neprilysin gene in sporadic Alzheimer's disease in Chinese persons J Gerontol A Biol Sci Med Sci 2005, 60(3):301-306. 15860464 15860464
34. Helisalmi S Hiltunen M Vepsalainen S Iivonen S Mannermaa A Lehtovirta M Koivisto AM Alafuzoff I Soininen H Polymorphisms in neprilysin gene affect the risk of Alzheimer's disease in Finnish patients J Neurol Neurosurg Psychiatry 2004, 75(12):1746-1748. 15548496 15548496 1738829
35. Sakai A Ujike H Nakata K Takehisa Y Imamura T Uchida N Kanzaki A Yamamoto M Fujisawa Y Okumura K et al.: Association of the Neprilysin gene with susceptibility to late-onset Alzheimer's disease Dement Geriatr Cogn Disord 2004, 17(3):164-169. 14739539 14739539
36. Clarimon J Munoz FJ Boada M Tarraga L Sunyer J Bertranpetit J Comas D Possible increased risk for Alzheimer's disease associated with neprilysin gene J Neural Transm 2003, 110(6):651-657. 12768360 12768360
37. Dolev I Michaelson DM A nontransgenic mouse model shows inducible amyloid-beta (Abeta) peptide deposition and elucidates the role of apolipoprotein E in the amyloid cascade Proc Natl Acad Sci USA 2004, 101(38):13909-13914. 15365176 15365176 518852
38. Marr RA Rockenstein E Mukherjee A Kindy MS Hersh LB Gage FH Verma IM Masliah E Neprilysin gene transfer reduces human amyloid pathology in transgenic mice J Neurosci 2003, 23(6):1992-1996. 12657655 12657655
39. Iwata N Mizukami H Shirotani K Takaki Y Muramatsu S Lu B Gerard NP Gerard C Ozawa K Saido TC Presynaptic localization of neprilysin contributes to efficient clearance of amyloid-beta peptide in mouse brain J Neurosci 2004, 24(4):991-998. 14749444 14749444
40. Hemming ML Patterson M Reske-Nielsen C Lin L Isacson O Selkoe DJ Reducing amyloid plaque burden via ex vivo gene delivery of an Abeta-degrading protease: A novel therapeutic approach to Alzheimer disease PLoS Med 2007, 4(8):e262. 17760499 17760499 1952204
41. Rockenstein E Torrance M Adame A Mante M Bar-on P Rose JB Crews L Masliah E Neuroprotective effects of regulators of the glycogen synthase kinase-3beta signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation J Neurosci 2007, 27(8):1981-1991. 17314294 17314294
42. Leissring MA Farris W Chang AY Walsh DM Wu X Sun X Frosch MP Selkoe DJ Enhanced proteolysis of beta-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death Neuron 2003, 40(6):1087-1093. 14687544 14687544
43. Mohajeri MH Wollmer MA Nitsch RM Abeta 42-induced increase in neprilysin is associated with prevention of amyloid plaque formation in vivo J Biol Chem 2002, 277(38):35460-35465. 12105192 12105192
44. Saito T Iwata N Tsubuki S Takaki Y Takano J Huang SM Suemoto T Higuchi M Saido TC Somatostatin regulates brain amyloid beta peptide Abeta42 through modulation of proteolytic degradation Nat Med 2005, 11(4):434-439. 15778722 15778722
45. Lazarov O Robinson J Tang YP Hairston IS Korade-Mirnics Z Lee VM Hersh LB Sapolsky RM Mirnics K Sisodia SS Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice Cell 2005, 120(5):701-713. 15766532 15766532
46. Farris W Schutz SG Cirrito JR Shankar GM Sun X George A Leissring MA Walsh DM Qiu WQ Holtzman DM et al.: Loss of neprilysin function promotes amyloid plaque formation and causes cerebral amyloid angiopathy Am J Pathol 2007, 171(1):241-251. 17591969 17591969 1941603
47. Huang SM Mouri A Kokubo H Nakajima R Suemoto T Higuchi M Staufenbiel M Noda Y Yamaguchi H Nabeshima T et al.: Neprilysin-sensitive Synapse-associated Amyloid-beta Peptide Oligomers Impair Neuronal Plasticity and Cognitive Function J Biol Chem 2006, 281(26):17941-17951. 16636059 16636059
48. Marr RA Guan H Rockenstein E Kindy M Gage FH Verma I Masliah E Hersh LB Neprilysin regulates amyloid Beta peptide levels J Mol Neurosci 2004, 22(1-2):5-11. 14742905 14742905
49. Hong CS Goins WF Goss JR Burton EA Glorioso JC Herpes simplex virus RNAi and neprilysin gene transfer vectors reduce accumulation of Alzheimer's disease-related amyloid-beta peptide in vivo Gene Ther 2006, 13(14):1068-1079. 16541122 16541122
50. Nagy Z Esiri M Jobst K Morris J King E McDonald B Litchfield S Smith A Barneston L Smith A Relative roles of plaques and tangles in the dementia of Alzheimer's disease: Correlations using three sets of neuropathological criteria Dementia 1995, 6:21-31. 7728216 7728216
51. Sloane JA Pietropaolo MF Rosene DL Moss MB Peters A Kemper T Abraham CR Lack of correlation between plaque burden and cognition in the aged monkey Acta Neuropathol 1997, 94(5):471-478. 9386780 9386780
52. Rockenstein E Mallory M Mante M Sisk A Masliah E Early formation of mature amyloid-b proteins deposits in a mutant APP transgenic model depends on levels of Ab1-42 J neurosci Res 2001, 66:573-582. 11746377
53. Hsia AY Masliah E McConlogue L Yu G-Q Tatsuno G Hu K Kholodenko D Malenka RC Nicoll RA Mucke L Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models ProcNatlAcadSciUSA 1999, 96:3228-3233. 10077666
54. El-Amouri SS Zhu H Yu J Marr R Verma IM Kindy MS Neprilysin: An enzyme candidate to slow the progression of Alzheimer's disease Am J Pathol 2008, 172(5):1342-1354. 18403590 18403590 2329843
55. Borchelt D Thinakaran G Eckman C Lee M Davenport F Ratovitsky T Prada C Kim G Seekins S Yager D Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ1-42/1-40 ratio in vitro and in vivo Neuron 1996, 17:1005-1013. 8938131 8938131
56. Huang F Buttini M Wyss-Coray T McConlogue L Kodama T Pitas RE Mucke L Elimination of the class A scavenger receptor does not affect amyloid plaque formation or neurodegeneration in transgenic mice expressing human amyloid protein precursors Am J Pathol 1999, 155(5):1741-1747. 1866996 10550330
57. Forloni G Chiesa R Smiroldo S Verga L Salmona M Tagliavini F Angeretti N Apoptosis mediated neurotoxicity induced by chronic application of β amyloid fragment 25-35 NeuroReport 1993, 4:523-526. 8513131
58. Echeverria V Cuello AC Intracellular A-beta amyloid, a sign for worse things to come? Mol Neurobiol 2002, 26(2-3):299-316. 12428762 12428762
59. Iijima-Ando K Hearn SA Granger L Shenton C Gatt A Chiang HC Hakker I Zhong Y Iijima K Overexpression of neprilysin reduces alzheimer amyloid-beta42 (Abeta42)-induced neuron loss and intraneuronal Abeta42 deposits but causes a reduction in cAMP-responsive element-binding protein-mediated transcription, age-dependent axon pathology, and premature death in Drosophila J Biol Chem 2008, 283(27):19066-19076. 18463098 18463098
60. Turner AJ Isaac RE Coates D The neprilysin (NEP) family of zinc metalloendopeptidases: Genomics and function Bioessays 2001, 23(3):261-269. 11223883 11223883
61. Russo R Borghi R Markesbery W Tabaton M Piccini A Neprylisin decreases uniformly in Alzheimer's disease and in normal aging FEBS Lett 2005, 579(27):6027-6030. 16226260 16226260
62. Miners JS Van Helmond Z Chalmers K Wilcock G Love S Kehoe PG Decreased expression and activity of neprilysin in Alzheimer disease are associated with cerebral amyloid angiopathy J Neuropathol Exp Neurol 2006, 65(10):1012-1021. 17021406 17021406
63. Hersh LB Peptidases, proteases and amyloid beta-peptide catabolism Curr Pharm Des 2003, 9(6):449-454. 12570808
64. Miyoshi H Blomer U Takahashi M Gage FH Verma IM Development of a self-inactivating lentivirus vector J Virol 1998, 72(10):8150-8157. 9733856 9733856 110156
65. Tiscornia G Singer O Verma IM Design and cloning of lentiviral vectors expressing small interfering RNAs Nat Protoc 2006, 1(1):234-240. 17406238 17406238
66. Dull T Zufferey R Kelly M Mandel RJ Nguyen M Trono D Naldini L A third-generation lentivirus vector with a conditional packaging system J Virol 1998, 72(11):8463-8471. 9765382 9765382 110254
67. Masliah E Rockenstein E Veinbergs I Sagara Y Mallory M Hashimoto M Mucke L beta-amyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease Proc Natl Acad Sci USA 2001, 98(21):12245-12250. 11572944 11572944 59799
68. Rockenstein E Mante M Alford M Adame A Crews L Hashimoto M Esposito L Mucke L Masliah E High beta-secretase activity elicits neurodegeneration in transgenic mice despite reductions in amyloid-beta levels: implications for the treatment of Alzheimer disease J Biol Chem 2005, 280(38):32957-32967. 16027115 16027115
69. Masliah E Rockenstein E Veinbergs I Mallory M Hashimoto M Takeda A Sagara Sisk A Mucke L Dopaminergic loss and inclusion body formation in alpha-synuclein mice: Implications for neurodegenerative disorders Science 2000, 287:1265-1269. 10678833 10678833
70. Rockenstein E Schwach G Ingolic E Adame A Crews L Mante M Pfragner R Schreiner E Windisch M Masliah E Lysosomal pathology associated with alpha-synuclein accumulation in transgenic models using an eGFP fusion protein J Neurosci Res 2005, 80(2):247-259. 15765523 15765523
71. Toggas S Masliah E Rockenstein E Mucke L Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice Nature 1994, 367:188-193. 8114918 8114918
72. Mucke L Abraham C Ruppe M Rockenstein E Toggas S Alford M Masliah E Protection against HIV-1 gp120-induced brain damage by neuronal overexpression of human amyloid precursor protein (hAPP) JExpMed 1995, 181:1551-1556.