A butyrolactone derivative 3BDO alleviates memory deficits and reduces amyloid-β deposition in an aβpp/ps1 transgenic mouse model

Journal of Alzheimer's Disease

Volumn 30, Issue 3, 2012, Pages 531-543

  Wei, Lifei ^a   Yang, Hui ^a   Xie, Zhaohong ^a   Yang, Hongna ^a   Zhao, Cuiping ^a   Wang, Ping ^a   Xu, Shunliang ^a   Miao, Junying ^b   Zhaoc, Bao Xiang ^b   Bi, Jian Zhong ^a  

^a THE SECOND HOSPITAL OF SHANDONG UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

Author keywords

Alzheimer's disease; amyloid peptides; autophagy; A PP PS1 mouse; insulin degrading enzyme; neprilysin

Indexed keywords

3 BENZYL 5 [(2 NITROPHENOXY)METHYL]DIHYDROFURAN 2(3H)ONE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; INSULINASE; LACTONE DERIVATIVE; MAMMALIAN TARGET OF RAPAMYCIN; MEMBRANE METALLOENDOPEPTIDASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LONG TERM CARE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

EID: 84862895820     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-111985     Document Type: Article

References (70)

1. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356.
2. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, Luo Y, Fisher S, Fuller J, Edenson S, Lile J, Jarosinski MA, Biere AL, Curran E, Burgess T, Louis JC, Collins F, Treanor J, Rogers G, CitronM(1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741.
3. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, Von Figura K, Van Leuven F (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387-390.
4. Bates KA, Verdile G, Li QX, Ames D, Hudson P, Masters CL, Martins RN (2009) Clearance mechanisms of Alzheimer's amyloid-beta peptide: Implications for therapeutic design and diagnostic tests. Mol Psychiatry 14, 469-486.
5. Wirths O, Multhaup G, Bayer TA (2004) A modified betaamyloid hypothesis: Intraneuronal accumulation of the betaamyloid peptide -the first step of a fatal cascade. J Neurochem 91, 513-520.
6. Verdile G, Fuller S, Atwood CS, Laws SM, Gandy SE, Martins RN (2004) The role of beta amyloid in Alzheimer's disease: Still a cause of everything or the only one who got caught? Pharmacol Res 50, 397-409.
7. Adlard PA, James SA, Bush AI, Masters CL (2009) beta-Amyloid as a molecular therapeutic target in Alzheimer's disease. Drugs Today (Barc) 45, 293-304.
8. Hamaguchi T, Ono K, YamadaM(2006) Anti-amyloidogenic therapies: Strategies for prevention and treatment of Alzheimer's disease. Cell Mol Life Sci 63, 1538-1552.
9. Funderburk SF, Marcellino BK, Yue Z (2010) Cell selfeating (autophagy) mechanism in Alzheimer's disease. Mt Sinai J Med 77, 59-68.
10. Yu WH, Kumar A, Peterhoff C, Shapiro Kulnane L, Uchiyama Y, Lamb BT, Cuervo AM, Nixon RA (2004) Autophagic vacuoles are enriched in amyloid precursor protein-secretase activities: Implications for beta-amyloid peptide over-production and localization in Alzheimer's disease. Int J Biochem Cell Biol 36, 2531-2540.
11. Nixon RA,Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM (2005) Extensive involvement of autophagy in Alzheimer disease: An immuno-electron microscopy study. J Neuropathol Exp Neurol 64, 113-122.
12. Yu WH, Cuervo AM, Kumar A, Peterhoff CM, Schmidt SD, Lee JH, Mohan PS, Mercken M, Farmery MR, Tjernberg LO, Jiang Y, Duff K, Uchiyama Y, Naslund J, Mathews PM, Cataldo AM, Nixon RA (2005) Macroautophagy -a novel Beta-amyloid peptide-generating pathway activated in Alzheimer's disease. J Cell Biol 171, 87-98.
13. Wang H, Ma J, Tan Y, Wang Z, Sheng C, Chen S, Ding J (2010) Amyloid-beta1-42 induces reactive oxygen speciesmediated autophagic cell death in U87 and SH-SY5Y cells. J Alzheimers Dis 21, 597-610.
14. Huang B, Meng N, Zhao B, Zhao J, Zhang Y, Zhang S, Miao J (2009) Protective effects of a synthesized butyrolactone derivative against chloroquine-induced autophagic vesicle accumulation and the disturbance of mitochondrial membrane potential and Na+, K+-ATPase activity in vascular endothelial cells. Chem Res Toxicol 22, 471-475.
15. Yang S, Wang S, Peng N, Xie Z, Wang P, Zhao C, Wei L, Yang H, Zhao B, Miao J, Bi J (2011) Butyrolactone derivative 3-benzyl-5-((2-nitrophenoxy) methyl)-dihydrofuran-2(3H)-one protects against amyloid-beta peptides-induced cytotoxicity in PC12 cells. J Alzheimers Dis 28, 345-356.
16. Zhang W, Hao J, Liu R, Zhang Z, Lei G, Su C, Miao J, Li Z (2011) Soluble Abeta levels correlate with cognitive deficits in the 12-month-old APPswe/PS1dE9 mouse model of Alzheimer's disease. Behav Brain Res 222, 342-350.
17. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, FroschMP(2006) Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24, 516-524.
18. Ruan L, Kang Z, Pei G, Le Y (2009) Amyloid deposition and inflammation in APPswe/PS1dE9 mouse model of Alzheimer's disease. Curr Alzheimer Res 6, 531-540.
19. Savonenko A, Xu GM, Melnikova T, Morton JL, Gonzales V, Wong MP, Price DL, Tang F, Markowska AL, Borchelt DR (2005) Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: Relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 18, 602-617.
20. O'Leary TP, Brown RE (2009) Visuo-spatial learning and memory deficits on the Barnes maze in the 16-month-old APPswe/PS1dE9 mouse model of Alzheimer's disease. Behav Brain Res 201, 120-127.
21. Zong Yy, Wang Xy, Wang Hl, Liu Yl, Huang L, Ma Cm, Zhang Lf, Qin C (2008) Continuous analysis of senile plaque and behaviour in APPswe/PS-E9 double-transgenic gene mouse model of Alzheimer disease. Chin J Comp Med 18, 8-14.
22. Sha L, Zhao B-X, Fan C-D, Tan W, Li X, Miao J-Y (2006) Synthesis and primary evaluation of lung cancer cell growth inhibitory activity of novel 3-arylmethyl-5-aroxymethylbutyrolactones. Chin J Org Chem 26, 537-541.
23. Vorhees CV,Williams MT (2006) Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1, 848-858.
24. JanusC(2004) Search strategies used by APP transgenic mice during navigation in the Morris water maze. Learn Mem 11, 337-346.
25. Spilman P, Podlutskaya N, Hart MJ, Debnath J, Gorostiza O, Bredesen D, Richardson A, Strong R, Galvan V (2010) Inhibition ofmTORby rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One 5, e9979.
26. Johnson-Wood K, Lee M, Motter R, Hu K, Gordon G, Barbour R, Khan K, Gordon M, Tan H, Games D, Lieberburg I, Schenk D, Seubert P, McConlogue L (1997) Amyloid precursor protein processing andAbeta42 deposition in a transgenic mouse model of Alzheimer disease. Proc Natl Acad Sci U S A 94, 1550-1555.
27. Wengenack TM, Whelan S, Curran GL, Duff KE, Poduslo JF (2000) Quantitative histological analysis of amyloid deposition in Alzheimer's double transgenic mouse brain. Neuroscience 101, 939-944.
28. Miners JS, Verbeek MM, Rikkert MO, Kehoe PG, Love S (2008) Immunocapture-based fluorometric assay for the measurement of neprilysin-specific enzyme activity in brain tissue homogenates and cerebrospinal fluid. J Neurosci Methods 167, 229-236.
29. Miners JS, Kehoe PG, Love S (2008) Immunocapture-based fluorometric assay for the measurement of insulin-degrading enzyme activity in brain tissue homogenates. J Neurosci Methods 169, 177-181.
30. Miners JS, van Helmond Z, Kehoe PG, Love S (2010) Changes with age in the activities of beta-secretase and the Abeta-degrading enzymes neprilysin, insulin-degrading enzyme and angiotensin-converting enzyme. Brain Pathol 20, 794-802.
31. Galvan V, Zhang J, Gorostiza OF, Banwait S, HuangW, Ataie M, Tang H, Bredesen DE (2008) Long-term prevention of Alzheimer's disease-like behavioral deficits in PDAPP mice carrying a mutation in Asp664. Behav Brain Res 191, 246-255.
32. Puttfarcken PS, Manelli AM, Neilly J, Frail DE (1996) Inhibition of age-induced beta-amyloid neurotoxicity in rat hippocampal cells. Exp Neurol 138, 73-81.
33. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
34. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14, 837-842.
35. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C,Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4, 97-100.
36. Dominguez DI, Hartmann D, De Strooper B (2004) BACE1 and presenilin: Two unusual aspartyl proteases involved in Alzheimer's disease. Neurodegener Dis 1, 168-174.
37. Meilandt WJ, Cisse M, Ho K, Wu T, Esposito LA, Scearce-Levie K, Cheng IH, Yu GQ, Mucke L (2009) Neprilysin overexpression inhibits plaque formation but fails to reduce pathogenic Abeta oligomers and associated cognitive deficits in human amyloid precursor protein transgenic mice. J Neurosci 29, 1977-1986.
38. Poirier R,WolferDP,Welzl H,Tracy J, GalsworthyMJ, Nitsch RM, Mohajeri MH (2006) Neuronal neprilysin overexpression is associated with attenuation of Abeta-related spatial memory deficit. Neurobiol Dis 24, 475-483.
39. Qiu WQ, Walsh DM, Ye Z, Vekrellis K, Zhang J, Podlisny MB, Rosner MR, Safavi A, Hersh LB, Selkoe DJ (1998) Insulin-degrading enzyme regulates extracellular levels of amyloid beta-protein by degradation. J BiolChem273, 32730-32738.
40. Vekrellis K, Ye Z, Qiu WQ, Walsh D, Hartley D, Chesneau V, Rosner MR, Selkoe DJ (2000) Neurons regulate extracellular levels of amyloid beta-protein via proteolysis by insulin-degrading enzyme. J Neurosci 20, 1657-1665.
41. Wang W, Liu X, Zhao J, Zhao B, Zhang S, Miao J (2007) A novel butyrolactone derivative inhibited apoptosis and depressed integrin beta4 expression in vascular endothelial cells. Bioorg Med Chem Lett 17, 482-485.
42. Wang W, Liu X, Zhang Y, Zhao J, Zhao B, Zhang S, Miao J (2007) Both senescence and apoptosis induced by deprivation of growth factors were inhibited by a novel butyrolactone derivative through depressing integrin beta4 in vascular endothelial cells. Endothelium 14, 325-332.
43. Meng N, Zhao J, Zhao B, Cheng Y,WangW, Zhang Y, Zhang S, Miao J (2008) A novel butyrolactone derivative inhibited smooth muscle cell migration and proliferation and maintained endothelial cell functions through selectively affecting Na, K-ATPase activity and mitochondria membrane potential during in vitro angiogenesis. J Cell Biochem 104, 2123-2130.
44. Caccamo A, Majumder S, Richardson A, Strong R, Oddo S (2010) Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: Effects on cognitive impairments. J Biol Chem 285, 13107-13120.
45. Mizushima N, Yoshimori T (2007) How to interpret LC3 immunoblotting. Autophagy 3, 542-545.
46. Itakura E, Mizushima N (2011) p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J Cell Biol 192, 17-27.
47. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171, 603-614.
48. Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140, 313-326.
49. Jaeger PA,Wyss-Coray T (2009) All-you-can-eat: Autophagy in neurodegeneration and neuroprotection. Mol Neurodegener 4, 16.
50. Selkoe DJ (2001) Clearing the brain's amyloid cobwebs. Neuron 32, 177-180.
51. 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 beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proc Natl Acad Sci U S A 100, 4162-4167.
52. Leissring MA, FarrisW, ChangAY,Walsh DM,WuX, Sun X, Frosch MP, Selkoe DJ (2003) Enhanced proteolysis of betaamyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 40, 1087-1093.
53. Cook DG, Leverenz JB, McMillan PJ, Kulstad JJ, Ericksen S, Roth RA, Schellenberg GD, Jin LW, Kovacina KS, Craft S (2003) Reduced hippocampal insulin-degrading enzyme in late-onset Alzheimer's disease is associated with the apolipoprotein E-epsilon4 allele. Am J Pathol 162, 313-319.
54. Kim M, Hersh LB, Leissring MA, Ingelsson M, Matsui T, Farris W, Lu A, Hyman BT, Selkoe DJ, Bertram L, Tanzi RE (2007) Decreased catalytic activity of the insulin-degrading enzyme in chromosome 10-linked Alzheimer disease families. J Biol Chem 282, 7825-7832.
55. Madani R, Poirier R, Wolfer DP, Welzl H, Groscurth P, Lipp HP, Lu B, El Mouedden M, Mercken M, Nitsch RM, MohajeriMH( 2006) Lack of neprilysin suffices to generate murine amyloid-like deposits in the brain and behavioral deficit in vivo. J Neurosci Res 84, 1871-1878.
56. Iwata N, Tsubuki S, Takaki Y, Shirotani K, Lu B, Gerard NP, Gerard C, Hama E, Lee HJ, Saido TC (2001) Metabolic regulation of brain Abeta by neprilysin. Science 292, 1550-1552.
57. HamaE, Shirotani K, Masumoto H, Sekine-AizawaY, Aizawa H, Saido TC (2001) Clearance of extracellular and cellassociated amyloid beta peptide through viral expression of neprilysin in primary neurons. J Biochem 130, 721-726.
58. Iwata N, Mizukami H, Shirotani K, Takaki Y, Muramatsu S, Lu B, Gerard NP, Gerard C, Ozawa K, Saido TC (2004) Presynaptic localization of neprilysin contributes to efficient clearance of amyloid-beta peptide in mouse brain. J Neurosci 24, 991-998.
59. 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.
60. Spencer B, Marr RA, Rockenstein E, Crews L, Adame A, Potkar R, Patrick C, Gage FH, Verma IM, Masliah E (2008) Long-term neprilysin gene transfer is associated with reduced levels of intracellular Abeta and behavioral improvement in APP transgenic mice. BMC Neurosci 9, 109.
61. Iijima-Ando K, Hearn SA, Granger L, Shenton C, Gatt A, Chiang HC, Hakker I, Zhong Y, Iijima K (2008) Overexpression of neprilysin reduces Alzheimer amyloid-beta42 (Abeta42)-induced neuron loss and intraneuronal Abeta42 deposits but causes a reduction in cAMP-responsive elementbinding protein-mediated transcription, age-dependent axon pathology, and premature death in Drosophila. J Biol Chem 283, 19066-19076.
62. Liu Y, Studzinski C, Beckett T, MurphyMP, Klein RL, Hersh LB (2010) Circulating neprilysin clears brain amyloid. Mol Cell Neurosci 45, 101-107.
63. Ling D, Song HJ, Garza D, Neufeld TP, Salvaterra PM (2009) Abeta42-induced neurodegeneration via an age-dependent autophagic-lysosomal injury in Drosophila. PLoS One 4, e4201.
64. Lipinski MM, Zheng B, Lu T, Yan Z, Py BF, Ng A, Xavier RJ, Li C,Yankner BA, Scherzer CR,Yuan J (2010) Genome-wide analysis reveals mechanisms modulating autophagy in normal brain aging and in Alzheimer's disease. Proc Natl Acad Sci U S A 107, 14164-14169.
65. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118, 2190-2199.
66. Barnett A, Brewer GJ (2011) Autophagy in aging and Alzheimer's disease: Pathologic or protective? J Alzheimers Dis 25, 385-394.
67. Li L, Zhang X, Le W (2010) Autophagy dysfunction in Alzheimer's disease. Neurodegener Dis 7, 265-271.
68. Majumder S, Richardson A, Strong R, Oddo S (2011) Inducing autophagy by rapamycin before, but not after, the formation of plaques and tangles ameliorates cognitive deficits. PLoS One 6, e25416.
69. Sanchez-Varo R, Trujillo-Estrada L, Sanchez-Mejias E, Torres M, Baglietto-Vargas D, Moreno-Gonzalez I, De Castro V, Jimenez S, Ruano D, Vizuete M, Davila JC, Garcia-Verdugo JM, Jimenez AJ, Vitorica J, Gutierrez A (2011) Abnormal accumulation of autophagic vesicles correlates with axonal and synaptic pathology in young Alzheimer's mice hippocampus. Acta Neuropathol 123, 53-70.
70. Garelick MG, Kennedy BK (2011) TOR on the brain. Exp Gerontol 46, 155-163.